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Recent progress of the effect of environmental factors on Aspergillus flavus growth and aflatoxins production on foods

Recent progress of the effect of environmental factors on Aspergillus flavus growth and... The contamination of Aspergillus flavus and subsequent aflatoxins (AFs) has been considered as one of the most serious food safety problems due to their acute and chronic adverse effects on humans and animals. This review collects the available information from recent years on the effect of the major environmental factors such as water activity (a ), temperature, CO , and pH on the w 2 fungal growth, the expression of AFs-related genes, and AFs production by A. flavus on foods. In particular, the relationship between the relative expression of key regulatory (aflR and aflS) and structural genes (aflD, aflO, aflQ, etc.) and AFs production under different environmental conditions are collected and discussed. The information collected in this review can be used to design control strategies of A.  flavus and AFs contamination in practical applications, primarily during storage and processing. These data suggest that integrating various post-harvest methods with synergistic functions may be more efficient for the control of A. flavus growth and AFs production, although the individual environmental factors alone have an impact. Key words: Aspergillus flavus; aflatoxin; water activity; temperature; CO . growth retardation in children (Groopman et  al., 2008). Among Introduction AFs, aflatoxin B (AFB ) was the most toxic one. The main source 1 1 The moldy contamination of staple foods such as cereals has been of exposure to AFs is the ingestion of contaminated food and feed. regarded as one of the most serious food safety problems due to Therefore, the high threat of AFs to the health of humans and ani- their acute and chronic negative effects on humans and animals mals has resulted in strict legislative limits in most countries and (Medina et al., 2014). Certain molds such as Aspergillus flavus and regions of the world for AFs and AFB in a wide range of foodstuffs Aspergillus parasiticus grown in corn, peanuts, and nuts produce af- and feeds (Commission of the European Communities, 2010; US latoxins (AFs). AFs have been classified as carcinogens in Group 1 Food and Drug Administration, 2010). by the International Agency for Research on Cancer (IARC, 1993, Aspergillus flavus is the predominant fungal species contamin- 2002). They are estimated to induce up to 28% of the total world- ating foodstuffs and feeds and producing AFs worldwide. It is also wide cases of hepatocellular carcinoma (HCC), the most common the main contaminant during the food storage since its ability to form of liver cancer (Liu et  al., 2012; Wu, 2014). Moreover, AFs produce AFs and its potential to persist as a pathogen and saprophyte also inevitably cause acute intoxication, immune suppression, and © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 2 B. T ai et al. in the food supply before and after harvest (Lahouar et  al., 2015). is aimed at reviewing the effects of the major environmental factors Aspergillus flavus is a xerophilic fungus that has developed physio- on fungal growth and AFs production by A. avus fl . Several studies logical mechanisms that adapt to environmental stress factors like have revealed the effect of environmental factors on fungal growth, low water activity (a ), allowing them to compete and often dom- genes expression, and AFs production. In order to avoid duplication inate other fungal communities (Nierman, 2008; Medina et  al., with that presented by Medina et al. (2014), studies that displayed 2015). The competitive advantage is because its metabolic plasticity the effects of environmental factors in the above-mentioned review allows it to produce a range of extracellular hydrolases, secondary are not thoroughly discussed. The following subsections describe the metabolites, and volatiles (Magan and Aldred, 2007). Therefore, studies published after 2014 and papers not presented in the afore- preventing and controlling the fungal growth and AFs production mentioned review. This review may provide the basic data for opti- by A. avus fl are essential and urgent to ensure the food safety and mizing the environmental conditions to control AFs contamination security in the world. on foodstuffs and feeds, especially during the storage. To eliminate AFs contamination in food chain, the most useful and cost-effective strategy is to create an adverse environment for Effect of a and temperature on A. flavus growth, A.  avus fl growth and AFs production. The growth of A.  avus fl gene expression, and AFs production on grains at the phenotypic level and the AFs production were observed to be associated with several environmental factors such as a , tem- Plenty of literatures have reported that the two key environmental perature, storage time, composition of the substrate, carbon and parameters, a and temperature, play important roles in modulating nitrogen source, pH, light, content of oxygen (O ) and carbon di- the A. avus fl growth and AFs production on foods (O’Brian et  al., oxide (CO ), loss of grains’ integrity caused by insects or mechan- 2007; Schmidt-Heydt et al., 2009, 2010; Yu et al., 2011; Marroquín- ical/thermal damage, and the interaction between fungal species Cardona et al., 2014; Bai et al., 2015). Among foods, grains are the that share the same ecological environment (Dantigny et al., 2005; most susceptible to the infection of A.  avus fl and the subsequent Vaamonde et al., 2006; Astoreca et al., 2014; Medina et al., 2015). AFs contamination (Guo et  al., 1998). Regarding AFs production, Regarding abiotic factors, a and temperature and their interactions various grains have a different sensitivity to a and temperature. w w have been demonstrated to be the major aetiological determinants Moreover, on the same grain, the optimal conditions for AFs produc- in regulating fungal growth and secondary metabolites production tion were significantly influenced by the A. avus fl strains, incubation (Mannaa and Kim, 2017; Medina et al., 2017). As an aerobic fungus, time and status of grains, etc. A.  avus fl growth and subsequent AFs production are highly influ- Mannaa and Kim (2018) investigated the effects of different rela- enced by CO with certain levels (Peleg et  al., 1988; Mousa et  al., tive humidities (RHs; 12, 44, 76, and 98%) and temperatures (10, 20, 2016). AFs are biosynthesized by 29 genes located in a 75 Kb gene 30, and 40°C) on major grain fungal populations including A. avus fl cluster in A.  avus fl , including the two regulatory genes (aflS and and some other fungi. They indicated that the populations of all aflR) and the structural genes such as aflD, aflM, and aflO (Liu et al., tested fungi in inoculated rice grains were significantly enhanced by 2017). The biosynthesis of AFs is also regulated by genes encoding both increased RH and temperature. In addition, multiple linear re- the velvet proteins such as veA and laeA, as well as developmental gression analysis revealed that one unit increase of temperature re- genes modulating morphology, conidiation, or sclerotia formation sulted in greater effects than that of RH on fungal populations. like brlA and abaA (Caceres et  al., 2016). Some oxidative stress- Mousa et al. (2013) conducted a study to model the radial growth related genes and cellular signal mediator genes such as rasA, msnA, rate and to assess AFs production by A.  avus fl as a function of a mtfA, and oxylipin’s biosynthetic genes (Tsitsigiannis and Keller, 0.82–0.92 and temperature 12 –42°C on polished and brown rice. 2007); G-protein receptor genes (Affeldt et al., 2014); and osmotic- They found that the brown rice is more susceptible to fungal inva- adaptation response gene sakA (Tumukunde et  al., 2019) can also sion and AFs production than polished rice. The optimum conditions influence AFs biosynthesis (Caceres et al., 2016). for A. avus fl growth and AFs production in brown rice were both at The expression of AF pathway genes is also influenced by some 0.92 a and 30°C. Fungal growth and AFs were undetectable at 0.82 environmental factors. In particular, the a × temperature interactions a on polished rice while they were both detected at this a under w w w are related to the ratio of the two key regulatory genes (aflS/aflR). 25–35°C on brown rice. At the temperature range of 25–30°C, the And the higher ratio of aflS/aflR would relate to the higher level minimum a values for AFs production on polished rice and brown of AFs production (Schmidt-Heydt et  al., 2009, 2010; Abdel-Hadi rice were 0.84 and 0.82, respectively. The highest levels of AFs were et  al., 2010, 2012; Medina et  al., 2014). Tumukunde et  al. (2019) observed at the highest a 0.90–0.92 at 20°C after 21 days of incu- indicated that low a was negatively related to the production of bation on both types of rice. However, at 7 and 14 days of incuba- AFB on corn and peanut kernels. Low a reduced the expression tion, the highest level of AFs was observed at a 0.92 and 30°C on 1 w w of AfsakA, which affected the conidiation and AFs biosynthesis. polished rice. On brown rice, the optimal condition for AFs pro- Moreover, the expression of 11 development-related genes increased duction at 7 and 14 days of incubation was a 0.92 × 25°C and a w w under 0.99 a treatment (Zhang et al., 2014). As for high tempera- 0.92 × 30°C, respectively. When temperature reached to 40°C, only ture, aflS and aflR were inhibited. The expression level of aflS/aflR a small amount of AFs were detected during the 3 weeks of incuba- seems to control the transcriptional activation of the AFs cluster (Yu tion, and both types of rice were only detectable at 0.92 a . et al., 2011). Compared with 37°C, the transcript abundance of 30 Similarly, Choi et al. (2015) showed that brown Korean rice was AFs biosynthesis genes was much higher at 30°C, and most genes sensitive to A.  avus fl growth and AF production compared with were up-regulated at both protein and transcription levels at 28°C rough Korean rice and white Korean rice. Regardless of the degree (Bai et  al., 2015). Taken together, the environmental factors have of milling of Korean rice, the optimum growth rate during 120 day significant effects on A. avus fl growth, the expression of AF biosyn- storage was at 85% RH/30°C and 97% RH/21°C. The highest thetic genes, and AFs production. population of A. avus fl and highest amount of AFB were observed Therefore, controlling the environmental factors is the most at 97% RH/21°C and on inoculated brown rice. Trace amounts of useful, cost-effective, practical, and green environmental strategy to AFB were detected during 10 day storage at 85% RH/21°C and in prevent and eliminate A. avus fl and AF contaminations. This paper all three non-inoculated types of rice. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 3 Lv et al. (2019) investigated the effect of a (0.92–0.96) and tem- Effect of a and temperature on A. flavus growth, perature (28–37°C) on the fungal growth and AFB production by gene expression, and AFs production on peanuts A. avus fl on polished rice and paddy. The results indicated that AFB 1 Peanut (Arachis hypogaea L.) is a globally important economic and production on polished rice can occur over a wider range of tem- oilseed crop worldwide. However, peanuts contamination with AFs perature × a levels than that on paddies. Aspergillus avus fl grew w and aflatoxigenic A. avus fl is regarded as the most serious problem better at 0.92–0.96 a and 28–37°C on polished rice, and the highest w in the world (Williams et  al., 2004; Liu et  al., 2017). Liu et  al. level of AFB was observed at 33°C and 0.96 a after 7 days of incu- 1 w (2017) investigated the effect of a (0.85–0.99) and temperature bation. In comparison to the optimal temperature of 33°C, all tested (15–42°C) on fungal growth, the expression of AF biosynthetic genes of A.  avus fl on polished rice were significantly up-regulated genes on un-autoclaved peanut kernels. The results indicated that at 25°C under 0.96 a . Compared with a 0.96, most of structural w w AFB production in peanut kernels can occur over a wider range genes of pathway were significantly down-regulated at a 0.90 and w of a and temperature compared with formula media and peanut 0.99 under 33°C, although two regulatory genes (aflR and aflS) media. Aspergillus flavus showed a lower growth rate at ≤0.85 a were up-regulated at a 0.90. For the A. avus fl growth on paddy, the w or ≤20°C. The optimal conditions for A. avus fl growth on peanuts optimal temperature and a were 37°C and 0.94 within the tested w kernels were 0.98 a and 37°C. The highest amount of AFB was w 1 range, respectively. Moreover, the highest concentration of AFB on 1 observed at 0.96 a and 28°C. paddy was observed at 0.92 a and 37°C after 7 days of incubation. w Moreover, the expression of AF-related and growth-related genes Lahouar et al. (2016) evaluated the impact of a (between 0.85 w was significantly modulated by a and temperature. At 0.92 a , 16 w w and 0.99), temperature (15, 25, and 37°C), and incubation time of the 25 genes had the highest expression levels at 28°C, whereas 9 (7, 14, 21, and 28 days) on A. avus fl growth and AFB production 1 genes had the highest expression levels at 37°C. In addition, all AF by three A.  avus fl isolates (8, 10, and 14)  inoculated on sorghum biosynthetic pathway genes were down-regulated at 42°C compared grains. Results showed that the optimal conditions for growth and with 37°C. Compared with 0.99 a , all the pathway genes and laeA AFB production were at 0.99 a and 37°C. For mycelial growth, the 1 w were up-expressed at a of 0.96 under 28°C. In particular, the ratio needed minimum a was 0.91 at 25 and 37°C. AFB accumulation w 1 of aflS/aflR was positively correlated with the AFB production. The could be avoided by storing sorghum at low a levels (≤0.91 a ) or w w expressions of laeA and brlA were positively associated with AFB at low temperature (15°C). production and fungal growth, respectively. Astoreca et al. (2014) studied the interaction of a (0.80–0.98), temperature (10–40°C), and incubation time (7, 14, 21, and 28 days) Effect of a and temperature on A. flavus growth on the co-production of AFB and cyclopiazonic acid (CPA) by and AFs production on tree nuts A. avus fl isolated from corn on Czapek yeast agar (CYA) and corn extract agar (CEM). They found the AFB production occurred more Tree nuts are commodities with moderate to high risk of AFs con- favourably on CYA while the maximum levels of CPA were observed tamination because they are produced at environmental conditions on CEM. The minimum level of a for both toxins production was favouring fungal growth and AFs production by aflatoxigenic fungi 0.83 with the tested a . The maximum amount of AFB was ob- especially A. avus fl (Arrus et  al., 2005; Gallo et  al., 2016). The in- w 1 served at 0.96 a and 30°C after 21 days of incubation, regardless cidence of AFs contamination in nuts is low; however, their levels of the isolates and media. Although they belong to three different vary widely and can produce high levels in a small number of nuts chemotypes: chemotype I  (AFB +/CPA+), chemotype III (AFB +/ (Campbell et al., 2003). 1 1 CPA−), and chemotype IV (AFB −/CPA+), respectively, the three iso- For the pistachio nuts, the highest amount of radial growth rate lates do not differ in the response to the environmental factors (a of A. avus fl and AFB production was obtained at 0.93 a and 30°C w 1 w and temperature). Moreover, the limiting and optimum conditions using a full factorial design with different moisture content levels for AFB and CPA production were similar on both media. (10, 15, 20, 25, and 30%) and incubation temperatures (10, 15, 20, Bernáldez et al. (2017) investigated the impact that interactions 25, 30, 37, and 42°C) (Marín et al., 2012). They also found that the between a and temperature may have on growth, the expression of limited AFs levels in pistachio nuts by European Commission would aflR, and AFB production by A. avus fl on a maize-based medium. be surpassed in a period as short as 1 month if pistachio nuts reach They found that there were some differences between lag phases 20°C, unless moisture content is ≤10%. However, this conclusion and growth rates of A. avus fl . The optimum condition for A. avus fl is not accurate because it was drawn from a single A. avus fl strain. growth on maize was 0.99 a and 30°C and the maximum AFB As we all know, the level of mycotoxins produced is highly variable w 1 production on maize was observed at 0.98 a and 30°C. Aspergillus even if only considering mycotoxin-producing strains in a species avus fl growth was completely inhibited at 0.90 a and 20°C. Both (Hua et al., 2012). a and temperature significantly influenced the relative expression Gallo et  al. (2016) evaluated the effects of different combin- of aflR gene and AFB production. However, the influences on AFB ations of a (0.90, 0.93, 0.96, and 0.99 a ) and temperature (20, 28, 1 1 w w production were not consistent with the effects on gene expression and 37°C) on A.  avus fl growth, AFB production, and expression and growth. These results suggested that the aflR expression was not of the two regulatory genes and two structural genes on an almond a good indicator of AFB production alone. Therefore, further mo- medium solidified with agar. The maximum amount of fungal bio- lecular studies of other AFs biosynthetic genes should be conducted. mass and AFB production was observed at 0.96 a and 28°C. At 1 w Based on the research by Krulj et  al., (2019), the optimal con- the driest tested conditions (0.90 and 0.93 a ), no fungal growth ditions for AFB biosynthesis were observed at 30°C in the tem- and AFB production were observed at 20°C. At 20 and 37°C, the 1 1 perature ranges of 15–37°C and the a levels at (0.85–0.99) in the yield of AFB was reduced by 70%–90% or completely suppressed, w 1 inoculated shell-less and shelled cereals. Moreover, the shell has a depending on a . Both regulatory genes (aflR and aflS) showed high higher amount of AFB in hull-less grain than the dehulled grains expression at maximum (28°C) and minimal (20 and 37°C) AFB 1 1 and the AFB content in the hull was even 10–170 times higher than production. In contrast, the two structural genes (aflD and aflO) the grain, indicating the shell has a protective effect. showed high expression only at the maximum AFB production 1 Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 4 B. T ai et al. (28°C and 0.96–0.99 a ). Based on this, temperature appears to be temperature. Regarding A.  parasiticus, the highest and lowest ex- a key factor affecting AFs production, which was strictly correlated pression values of both regulatory genes were observed at 0.95 a with the expression of the structural genes (aflD and aflO), but not and 0.85 a , respectively. In contrast, the expression of aflP gene in to that of the two regulatory genes. This result suggests that some both species was stimulated at low temperature and a . Furthermore, post-transcriptional regulatory processes are involved in modulating a strong correlation between the relative expression of aflR and aflS AFs biosynthesis. gene and AFs production was obtained under environmental condi- Prencipe et al. (2018) evaluated the drying temperatures (from 30 tions which simulate dry-cured ham ripening. to 50°C) on A. avus fl growth and AFs production in chestnuts and indicated that the optimal temperature for fungal growth was 30°C, Effect of other environmental factors on A. flavus whereas the highest concentrations of AFB and AFB were obtained 1 2 growth and AFs production on food at 40°C. At this temperature, A. avus fl was under suboptimal condi- In addition to a and temperature, there are more environmental tions for growth (0.78 a ), but AFs biosynthesis was under the op- parameters that have been investigated for the influences on the timal conditions. When the drying temperatures reached 45–50°C, growth and AFs production by A. avus fl in many studies. It has been AFs production was completely inhibited. Drying at 45°C for 7 days reported that pH, CO level, and light treatment also exhibit signifi- (0.64 a ) could be a promising strategy to effectively control both cant effects on fungal growth and AFs production (Schmidt-Heydt A. flavus growth and AFs production. et al., 2008; Oms-Oliu et al., 2010; Castellari et al., 2015). Regarding pH, Casquete et  al. (2017) investigated the effect of Effect of a and temperature on A. flavus pH (5.0, 5.5, and 6.0), a (0.90, 0.95, and 0.99), and temperature growth, gene expression, and AFs production on (15, 20, 25, and 30°C) on the lag phases, growth, and AFs produc- other foods tion of three aflatoxigenic A. avus fl strains (CQ7, CQ8, and CG103) on cheese-based medium. The results showed that the behaviour of Recently, there are some researches that reported the effect of a and A. avus fl strains was affected by pH, a , and temperature; however, temperature on the fungal growth and AFs production by A. avus fl A. avus fl growth was less affected by pH than the others. The CQ7 on other foods. In whole black peppercorns (Piper nigrum L.), the strain exhibited maximum growth at pH 5.5, 0.99 a , and 25°C. growth and AFs production of three A.  avus fl isolates and one However, for the CQ8 and CQ103 strains, there was no difference A.  parasiticus isolate were investigated using a full factorial design between pH 5.5 and 6.0. The maximum AFs production on the with seven a levels (0.826–0.984) and three temperatures (22, 30, cheese-based medium occurred at pH 5.0, 0.95 a , and 25 or 30°C, and 37°C) (Yogendrarajah et al., 2016). Among secondary models, depending on the strain. Kosegarten et al. (2017) also indicated that the extended Gibson model was the best model to describe the com- an increase in pH value between 3.5 and 6.5 resulted in an increase bined effect of a and temperature on the growth rate of both fungal in the growth of A. flavus. species in peppercorns. The highest population of A. avus fl occurred For CO level, Mousa et  al. (2016) illustrated that the growth at 0.92 a and 30°C, and the maximum yield of AFB was also ob- w 1 of A. avus fl and AFs production was highly influenced by the CO served under this condition based on diverse secondary models. The level (20%–80%) on paddy. In general, fungal growth rates and estimated minimum a and temperature for the growth of A. avus fl AFs production were negatively correlated with CO , whereas the were 0.73–0.76 and 11–16°C, respectively. High variability in AFs lag phase durations were positively correlated with CO . However, production of different aflatoxigenic species limited the modelling the highest tested CO level (80%) could not completely inhibit the of AFs production. Based on the research of Yogendrarajah et  al. fungi growth. Under 0.98 a , 20% and 80% CO caused at least (2016), the limiting a and temperature should be considered to pre- w 2 59% and 88% reduction in growth and 47% and 97% reduction vent the aflatoxigenic fungal species growth and AFs production in in AFs production, respectively. In addition, a significant inhibition food during storage. of growth was observed at 75% CO at both 0.95 and 0.92 a on Peromingo et  al. (2016) evaluated that the interaction between 2 w agar medium. The population of A. avus fl isolated from grains was a (0.85, 0.90, and 0.95) and temperature (10, 15, 20, and 25°C) inhibited at up to 75% CO (Giorni et al., 2008). Giorni et al. (2008) may occur on lag phases prior to growth, growth rates, and AFs also has reported that the moisture maize treated with 25% CO was production by two strains of each A.  parasiticus and A.  avus fl on sufficient to effectively reduce the development of A. avus fl , but at cured meat over 12 days. Aspergillus flavus CBS 573.65 had shorter least 50% CO was required to significantly reduce the synthesis of lag phases than A.  parasiticus CECT 2 688; however, the growth AFs. Therefore, controlling pH and CO levels during manufacturing rates of the two strains were similar. The optimum growth and AFs and storage is an effective control strategy to avoid the contamin- production occurred at 0.95 a and 25°C. At 10°C and all tested ation of A. flavus and subsequent AFs (Chulze, 2010). a , no growth occurred for both species. Both species produced AFs when the a and temperature were a ≥ 0.90 and ≥15°C, respect- w w ively. Although similar AFB production characteristics were found Discussion and Conclusions between the two species, the concentration of this toxin produced by A. flavus was much higher than that of A. parasiticus. These previous studies have indicated that several environmental To elucidate the relationship between the relative expression factors play important roles in regulating fungal growth, the expres- of AFs-related genes and AFs production, Peromingo et  al. (2017) sion of AF biosynthetic genes, and AFs production by A. avus fl and evaluated the effect of different a and temperatures on the temporal A.  parasiticus. Especially, a and temperature are limiting factors w w relative expression of three genes in AFs biosynthesis cluster and during storage (Liu et al., 2017). Therefore, this review summarizes their correlation with AFs production on dry-cured ham-based me- the different ranges of a and temperature and the optimal condition dium by A. avus fl and A. parasiticus. In general, the expressions of for A. avus fl growth and AFs production on different food substrate the regulatory aflR and aflS genes were similar and much lower than and formula media (Figures 1 and 2). As shown in the two figures, the expression of the structural aflP gene. The expression of aflR and the optimal conditions of a × temperature for A.  avus fl growth aflS genes in A. avus fl increased over a decrease of a regardless of and AFs production vary on different foods or formula medium (Lv w Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 5 Figure 1. Comparison of a and temperature ranges and the optimal Figure 2. Comparison of a and temperature ranges and the optimal conditions (the black line) for the growth of A.  flavus in different food conditions (the black line) for the aflatoxin (AF) production in different food matrices and formula medium. (A) Aspergillus flavus growth at different a . matrices and formula medium. (A) AF production at different a . (B) AF (B) Aspergillus flavus growth at different temperatures. production at different temperatures. aflS were highlighted. On YES medium, the down-regulation of aflR et  al., 2019). On yeast extract sucrose (YES) medium, the suitable and aflS induced the inhibition of AFs production (Yu et al., 2011). temperatures for AFB production were 25–30°C at 0.99 a , whereas 1 w And the decrease in the expression ratio of aflS/aflR leads to tran- the range changed to 30–35°C at 0.95 a (Abdel-Hadi et al., 2012). scription inactivation of AFs cluster. Similar findings were obtained On un-autoclaved peanut kernels, the suitable temperatures for on un-autoclaved peanut kernels (Liu et  al., 2017). At 42°C, the AFB production were 0.92–0.96 a and 25–33°C, and the highest 1 w lower ratio of aflS/aflR resulted in lower AFB production compared level of AFB was observed at 0.96 a and 28°C (Liu et al., 2017). 1 w 1 with 28 and 37°C. Similar findings were obtained on almond medium; the maximum In contrast, some literatures have reported that the aflR expres- fungal growth and AFB production were observed at 0.96 a and 1 w sion is not consistent with AFs production at several conditions. 28°C (Gallo et al., 2016). On un-autoclaved polished rice, high pro- On a maize-based medium, the influences of a and temperature duction of AFB was observed at 0.90–0.99 a and 25–33°C, and the 1 w w on AFB production were different with the expression of aflR gene maximum amount of AFB was obtained at 0.96 a and 33°C (Lv 1 w 1 (Bernáldez et al., 2017). On polished rice, the down-regulation of all et al., 2019). Moreover, these results suggest that the fungal growth the tested AFs structural genes at a 0.90 resulted in a low level of and AFs production on foods can occur over a wider range of a × w w AFB production compared with a 0.96, although aflR and aflS were temperature than on formula medium. The diversity of optimal con- 1 w both up-regulated (Lv et  al., 2019). Similar findings were reported ditions may be due to the differences in media structure and nutrient by O’Brian et al. (2007), who obtained an opposite relationship be- availability (Ahmad et al., 2013; Mousa et al., 2013). tween AFs biosynthesis and the expression of aflR and aflS. AFs pro- Compared with the investigations published before 2015, the re- duction was completely inhibited at 37°C although both regulatory cent publications pay more attention to the correlation between the genes were highly expression in liquid A  and M media. Schmidt- expression of AFs biosynthetic genes and AFs production. The re- Heydt et al. (2009) indicated that the transcription level of aflS was searchers attempt to get a good indicator of possible AFs contamin- high at >37°C under almost all a ranges tested, but the amount ation on foods by early detecting the expression of AFs-related genes. of AFs production was low on YES medium. These results suggest As the key regulatory genes in AFs biosynthesis gene cluster, aflR and Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 6 B. T ai et al. that some other molecular mechanisms, such as post-transcriptional 2008). It is important to notice that the residual O may be a limiting mechanism, were involved in modulating the transcriptional level of factor for fungal growth and AFs production under modified atmos- AFs structural genes and the subsequent AFs production. phere packaging (Taniwaki et al., 2009). Compared with the two regulatory genes aflR and aflS, the tran- The pH is also an important factor in determining A.  avus fl scriptional levels of some structural genes seem to have more strong growth and AFs production. Klich (2007) indicated that the increase correlation to AFs production. Gallo et al. (2016) indicated that the in pH (4–6) was related to the increase of A. avus fl growth, and the effect of environmental factors on AFs biosynthesis had a better expression of the AFs pathway gene was also affected by the pH of correlation to the transcriptional activation/inactivation of struc- the medium. In some foods such as fermented food, salted food, and tural genes (aflD and aflO) than the two regulatory genes. Similarly, canned food, fungal growth and AFs production can be controlled Abdel-Hadi et al. (2010) also obtained a good correlation between by adjusting pH values. However, there are some limitations on the aflD expression and AFB production by A.  avus fl in raw peanuts practical application of adjusting pH in most foods, especially the under different a levels. In addition, the significant differences be- grains and spices listed in this paper. tween the relative expression of aflD at different temperatures (28, In conclusion, the low a and temperature or the increase in the 37, and 42°C) were observed, resulting in the significant differences CO level alone is not effective for complete control of A.  avus fl in AFB production on peanut kernels (Liu et  al., 2017). On YES and AFs production. Integrating various post-harvest methods with medium, the expression profile of aflD, aflO, and aflP was consist- synergistic functions may be more efficient for the complete inhib- ently correlated with the ability of AFs production (Scherm et  al., ition of A.  avus fl growth and AFs production during storage and 2005). On polished rice, the structural genes (aflM, aflN, aflO, aflP, processing of foods. For example, reducing a is the prerequisite aflQ, aflU, and nadA) involved in the middle and late stages of AFs step to prevent A.  avus fl infection and AFs production, and con- pathway from VERA (Versicolorin A) to AFB were down-regulated trolling a and temperature and increasing the level of CO in the 1 w 2 at 37°C compared with 33°C under a 0.96 (Lv et  al., 2019). The atmosphere are useful strategies during storage. Good Agricultural lower expression of these structural genes led to the decrease of AFB Practices (GAP) and Good Processing Practices (GPP) represent pri- production. On peanuts kernels, a good positive correlation between mary preventive measures against A. avus fl and the subsequent AFs. the expression of aflQ, being involved in the final step of the AFs Integrating the two principles with the Hazard Analysis and Critical biosynthetic pathway and encoding an oxidoreductase, and AFB Control Point (HACCP) can be used efficiently (Mousa et al., 2016). level was observed under different a ’s and temperatures (Liu et al., A  better knowledge of the environmental factors governing fungal 2017). Taken together, these results suggest that an early detection of growth and AFs production provided in the above-mentioned recent the expression of some key structural genes (aflD, aflO, aflP, or aflQ) researches would help in establishing optimal guidelines in GAP and can be a better indicator of possible AFs contamination on foods GPP, preventive measures, and critical limits in HACCP plans. under different a ’s and temperatures compared with aflS and aflR. Besides modulating a and temperature, modified atmosphere Acknowledgements packaging is regarded as a promising food preservation technique because it integrates the control microbial activity and insects, which We gratefully acknowledge the financial support of National Key R&D tend to maintain the quality of the products and extend the shelf life Program of China (2016YFD0400105). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the with minimal application of chemicals (Taniwaki et al., 2009; Mousa manuscript. et al., 2016). CO was proved to retard the fungal growth and inhibit AFs production by A. avus fl . Taniwaki et  al. (2009) indicated that no fungal growth of A. avus fl was observed at 40% and 60% CO Conflict of Interest when O level was <0.5% while growth was observed on PDA and None declared. CYA at 20% CO . However, even at the lowest CO level (20%) 2 2 studied, the retarding effect of CO on the growth rate of A. avus fl was significant on paddy (Mousa et al., 2016). Overall, 55%–100% References reduction in fungal growth was achieved with CO treatment. On Abdel-Hadi,  A., Carter,  D., Magan,  N. (2010). Temporal monitoring of the moistened maize, modified atmospheres with 25%–50% CO only nor-1 (aflD) gene of Aspergillus flavus in relation to aflatoxin B produc- contributed to 30%–35% reduction in A. avus fl growth while as the tion during storage of peanuts under different water activity levels. Journal concentrations of CO increased up to 75%, the reduction of above of Applied Microbiology, 109: 1914–1922. 50% was obtained (Giorni et  al., 2008). The more reduction of Abdel-Hadi, A., Schmidt-Heydt, M., Parra, R., Geisen, R., Magan, N. (2012). fungal growth on paddy than maize with CO treatment may be due A systems approach to model the relationship between aflatoxin gene to the more resistance of paddy’s physical structure to the invading cluster expression, environmental factors, growth and toxin production fungi (Mousa et al., 2016). by Aspergillus flavus. Journal of the Royal Society, Interface, 9: 757–767. Besides fungal growth, AFs production was also significantly Affeldt, K. J., Carrig, J., Amare, M., Keller, N. P. (2014). Global survey of ca- inhibited by modified atmosphere with CO . Mousa et  al. (2016) nonical Aspergillus flavus G protein-coupled receptors. Mbio, 5: e01501– e01514. found that the reduction in AFs production on paddy with CO Ahmad, M., Ahmad, M. M., Hamid, R., Abdin, M. Z., Javed, S. (2013). Use of treatment (20%–80%) was in the range of 65.8%–98.0%, 70.4%– response surface methodology to study the effect of media composition on 94.6%, and 72.9%–96.8% at 0.98, 0.95, and 0.92 a , respectively. aflatoxin production by Aspergillus flavus. Mycotoxin Research, 29: 39–45. However, no significant reduction in AFs production on maize was Arrus, K., Blank, G., Abramson, D., Clear, R., Holley, R. A. (2005). Aflatoxin observed with modified atmosphere enriched with 25% CO and production by Aspergillus flavus in Brazil nuts. Journal Stored Products balanced with N (Giorni et al., 2008). With the application of 50% Research, 41(5): 513–527. and 75% CO , 46% and 58% overall reduction in AFs production Astoreca, A., Vaamonde, G., Dalcero, A., Marin, S., Ramos, A. (2014). Abiotic was observed, respectively. Additionally, on PDA or CYA enclosed factors and their interactions influence on the co-production of aflatoxin with a modified atmosphere with 20% CO and <0.5% residual B(1) and cyclopiazonic acid by Aspergillus avus fl isolated from corn. Food oxygen, no AFs production was observed for 30 days (Giorni et al., Microbiology, 38: 276–283. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 7 Bai, Y., et al. (2015). Integrative analyses reveal transcriptome-proteome cor- Krulj, J., et al. (2019). The effect of storage temperature and water activity on relation in biological pathways and secondary metabolism clusters in aflatoxin B1 accumulation in hull-less and hulled spelt grains. Journal of A. flavus in response to temperature. Scientific Reports, 5: 14582. the Science of Food and Agriculture, 99: 3703–3710. Bernáldez, V., Córdoba, J. J., Magan, N., Peromingo, B., Rodríguez, A. (2017). Lahouar, A., Crespo-Sempere, A., Marín, S., Saïd, S., Sanchis, V. (2015). Toxi- The influence of ecophysiological factors on growth, aflR, gene expression genic molds in Tunisian and Egyptian sorghum for human consumption. and aflatoxin B1 production by a type strain of Aspergillus flavus. LWT - Journal of Stored Products Research, 63: 57–62. Food Science and Technology, 83: 283–291. Lahouar, A., Marin, S., Crespo-Sempere, A., Saïd, S., Sanchis, V. (2016). Ef- Caceres,  I., et  al. (2016). Deciphering the anti-aflatoxinogenic properties of fects of temperature, water activity and incubation time on fungal growth eugenol using a large-scale q-PCR approach. Toxins, 8: 123. and aflatoxin B1 production by toxinogenic Aspergillus flavus isolates on Campbell, B. C., Molyneux, R. J., Schatzki, T. F. (2003). Current research on sorghum seeds. Revista Argentina De Microbiologia, 48: 78–85. reducing pre‐ and post‐harvest aflatoxin contamination of U.S.  almond, Liu, Y., Chang, C. C., Marsh, G. M., Wu, F. (2012). Population attributable pistachio, and walnut. Toxin Reviews, 22(2–3): 225–266. risk of aflatoxin-related liver cancer: systematic review and meta-analysis. Casquete,  R., Benito,  M.  J., Córdoba,  M.  G., Ruiz-Moyano,  S., Martín,  A. European Journal of Cancer (Oxford, England: 1990), 48: 2125–2136. (2017). The growth and aflatoxin production of Aspergillus flavus strains Liu, X., Guan, X., Xing, F., Lv, C., Dai, X., Liu, Y. (2017). Effect of water ac- on a cheese model system are influenced by physicochemical factors. tivity and temperature on the growth of Aspergillus flavus, the expression Journal of Dairy Science, 100: 6987–6996. of aflatoxin biosynthetic genes and aflatoxin production in shelled pea- Castellari, C. C., Cendoya, M. G., Marcos Valle, F. J., Barrera, V., Pacin, A. M. nuts. Food Control, 82: 325–332. (2015). [Extrinsic and intrinsic factors associated with mycotoxigenic Lv,  C., et  al. (2019). Interaction of water activity and temperature on the fungi populations of maize grains (Zea mays L.) stored in silobags in Ar- growth, gene expression and aflatoxin production by Aspergillus flavus on gentina]. Revista Argentina De Microbiologia, 47: 350–359. paddy and polished rice. Food Chemistry, 293: 472–478. Choi,  S., et  al. (2015). Behaviour of Aspergillus flavus and Fusarium Magan,  N., Aldred,  D. (2007). Post-harvest control strategies: minimizing graminearum on rice as affected by degree of milling, temperature, and mycotoxins in the food chain. International Journal of Food Microbiology, relative humidity during storage. Food Microbiology, 46: 307–313. 119: 131–139. Chulze,  S.  N. (2010). Strategies to reduce mycotoxin levels in maize during Mannaa, M., Kim, K. D. (2017). Influence of temperature and water activity storage: a review. Food Additives & Contaminants. Part A, Chemistry, on deleterious fungi and mycotoxin production during grain storage. Analysis, Control, Exposure & Risk Assessment, 27: 651–657. Mycobiology, 45: 240–254. Commission of the European Communities. (2010). Commission regulation Mannaa, M., Kim, K. D. (2018). Effect of temperature and relative humidity (EU) No 165/2010 of 26 February 2010 amending Regulation (EC) No on growth of Aspergillus and Penicillium spp. and biocontrol activity of 1881/2006 setting maximum levels for certain contaminants in foodstuffs Pseudomonas protegens AS15 against aflatoxigenic Aspergillus flavus in as regards aflatoxins. Official Journal of European Union, 50: 8–12. stored rice grains. Mycobiology, 46: 287–295. Dantigny, P., Guilmart, A., Radoi, F., Bensoussan, M., Zwietering, M. (2005). Marín,  S., Ramos,  A.  J., Sanchis,  V. (2012). Modelling Aspergillus flavus Modelling the effect of ethanol on growth rate of food spoilage moulds. growth and aflatoxins production in pistachio nuts. Food Microbiology, International Journal of Food Microbiology, 98: 261–269. 32: 378–388. Gallo, A., Solfrizzo, M., Epifani, F., Panzarini, G., Perrone, G. (2016). Effect Marroquín-Cardona,  A.  G., Johnson,  N.  M., Phillips,  T.  D., Hayes,  A.  W. of temperature and water activity on gene expression and aflatoxin bio- (2014). Mycotoxins in a changing global environment–a review. Food and synthesis in Aspergillus flavus on almond medium. International Journal Chemical Toxicology, 69: 220–230. of Food Microbiology, 217: 162–169. Medina,  A., et  al. (2017). Interactions between water activity and tempera- Giorni,  P., Battilani,  P., Pietri,  A., Magan,  N. (2008). Effect of a and CO ture on the Aspergillus avus fl transcriptome and aflatoxin B1 production. w 2 level on Aspergillus avus fl growth and aflatoxin production in high mois- International Journal of Food Microbiology, 256: 36–44. ture maize post-harvest. International Journal of Food Microbiology, 122: Medina,  A., Rodriguez,  A., Magan,  N. (2014). Effect of climate change on 109–113. Aspergillus flavus and aflatoxin B1 production. Frontiers in Microbiology, Groopman, J. D., Kensler, T. W., Wild, C. P. (2008). Protective interventions to 5: 348. prevent aflatoxin-induced carcinogenesis in developing countries. Annual Medina,  A., Schmidt-Heydt,  M., Rodríguez,  A., Parra,  R., Geisen,  R., Review of Public Health, 29: 187–203. Magan,  N. (2015). Impacts of environmental stress on growth, sec- Guo,  B.  Z., Brown,  R.  L., Lax,  A.  R., Cleveland,  T.  E., Russin,  J.  S., ondary metabolite biosynthetic gene clusters and metabolite production Widstrom, N. W. (1998). Protein profiles and antifungal activities of kernel of xerotolerant/xerophilic fungi. Current Genetics, 61: 325–334. extracts from corn genotypes resistant and susceptible to Aspergillus Mousa,  W., Ghazali,  F.  M., Jinap,  S., Ghazali,  H.  M., Radu,  S. (2013). avus fl . Journal of Food Protection, 61: 98–102. Modeling growth rate and assessing aflatoxins production by Aspergillus Hua, S. S., McAlpin, C. E., Chang, P. K., Sarreal, S. B. (2012). Characteriza- avus fl as a function of water activity and temperature on polished and tion of aflatoxigenic and non-aflatoxigenic Aspergillus avus fl isolates from brown rice. Journal of Food Science, 78: M56–M63. pistachio. Mycotoxin Research, 28: 67–75. Mousa, W., Ghazali, F. M., Jinap, S., Ghazali, H. M., Radu, S., Salama, A. E. R. International Agency for Research on Cancer. (1993). Some naturally occurring (2016). Temperature, water activity and gas composition effects on the substances: food items and constituents, heterocyclic aromatic amines and growth and aflatoxin production by Aspergillus flavus on paddy. Journal mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risks of Stored Products Research, 67: 49–55. to Humans, 56: 245–395. Nierman,  W.  T. (2008). Mycotoxin production and prevention of aflatoxin International Agency for Research on Cancer. (2002). Some traditional herbal contamination in food and feed. Aspergilli Genomics Medical Aspects medicines, some mycotoxins, naphthalene and styrene. IARC Monographs Biotechnology & Research Methods, 8(8): 84–88. on the Evaluation of Carcinogenic Risks to Humans, 82: 1–556. O’Brian, G. R., et al. (2007). The effect of elevated temperature on gene tran- Klich,  M.  A. (2007). Environmental and developmental factors influencing scription and aflatoxin biosynthesis. Mycologia, 99: 232–239. aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Oms-Oliu,  G., Martín-Belloso,  O., Soliva-Fortuny,  R. (2010). Pulsed light Mycoscience, 48(2): 71–80. treatments for food preservation. A  review. Food and Bioprocess Tech- Kosegarten,  C.  E., Ramírez-Corona,  N., Mani-López,  E., Palou,  E., López- nology, 3(1): 13–23. Malo, A. (2017). Description of Aspergillus flavus growth under the influ- Peleg,  Y., Stieglitz,  B., Goldberg,  I. (1988). Malic acid accumulation by ence of different factors (water activity, incubation temperature, protein Aspergillus avus fl . Applied Microbiology and Biotechnology, 28(1): 69– and fat concentration, pH, and cinnamon essential oil concentration) by 75. kinetic, probability of growth, and time-to-detection models. International Peromingo,  B., Rodríguez,  A., Bernáldez,  V., Delgado,  J., Rodríguez,  M. Journal of Food Microbiology, 240: 115–123. (2016). Effect of temperature and water activity on growth and aflatoxin Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 8 B. T ai et al. production by Aspergillus flavus and Aspergillus parasiticus on cured meat Tsitsigiannis,  D.  I., Keller,  N.  P. (2007). Oxylipins as developmental and model systems. Meat Science, 122: 76–83. host-fungal communication signals. Trends in Microbiology, 15: 109– Peromingo,  B., Rodríguez,  M., Delgado,  J., Andrade,  M.  J., Rodríguez,  A. 118. (2017). Gene expression as a good indicator of aflatoxin contamination in Tumukunde, E., Li, D., Qin, L., Li, Y., Shen, J. J., Wang, S. H., Yuan, J. (2019). dry-cured ham. Food Microbiology, 67: 31–40. Osmotic-adaptation response of sakA/hogA gene to aflatoxin biosyn- Prencipe,  S., Siciliano,  I., Gatti,  C., Gullino,  M., Garibaldi,  A., Spadaro,  D. thesis, morphology development and pathogenicity in Aspergillus avus fl . (2018). Chestnut drying is critical in determining Aspergillus flavus Toxins, 11: 41. growth and aflatoxin contamination. Toxins, 10(12): 530. US Food and Drug Administration (2010). Aflatoxin in Peanuts and Peanut Scherm, B., Palomba, M., Serra, D., Marcello, A., Migheli, Q. (2005). Detec- Products: 2010; CPG Sec. 570.375. Compliance Manuals. http://www.fda. tion of transcripts of the aflatoxin genes aflD, aflO, and aflP by reverse gov/ICECI/ComplianceManuals. Accessed 16 August 2019. transcription-polymerase chain reaction allows differentiation of aflatoxin- Vaamonde, G., Patriarca, A., Fernández Pinto, V. E. (2006). Effect of water ac- producing and non-producing isolates of Aspergillus flavus and Aspergillus tivity and temperature on production of aflatoxin and cyclopiazonic acid parasiticus. International Journal of Food Microbiology, 98: 201–210. by Aspergillus flavus in peanuts. Advances in Experimental Medicine and Schmidt-Heydt, M., Abdel-Hadi, A., Magan, N., Geisen, R. (2009). Complex Biology, 571: 225–235. regulation of the aflatoxin biosynthesis gene cluster of Aspergillus flavus in Williams, J. H., Phillips, T. D., Jolly, P. E., Stiles, J. K., Jolly, C. M., Aggarwal, D. relation to various combinations of water activity and temperature. Inter- (2004). Human aflatoxicosis in developing countries: a review of toxi- national Journal of Food Microbiology, 135: 231–237. cology, exposure, potential health consequences, and interventions. The Schmidt-Heydt, M., Magan, N., Geisen, R. (2008). Stress induction of myco- American Journal of Clinical Nutrition, 80: 1106–1122. toxin biosynthesis genes by abiotic factors. FEMS Microbiology Letters, Wu, F. (2014). Perspective: time to face the fungal threat. Nature, 516: S7. 284: 142–149. Yogendrarajah,  P., et  al. (2016). Mycotoxin production and predictive Schmidt-Heydt,  M., Rüfer,  C.  E., Abdel-Hadi,  A., Magan,  N., Geisen,  R. modelling kinetics on the growth of Aspergillus flavus and Aspergillus (2010). The production of aflatoxin B1 or G 1 by Aspergillus parasiticus parasiticus isolates in whole black peppercorns (Piper nigrum L). Inter- at various combinations of temperature and water activity is related to the national Journal of Food Microbiology, 228: 44–57. ratio of aflS to aflR expression. Mycotoxin Research, 26: 241–246. Yu, J., et al. (2011). Tight control of mycotoxin biosynthesis gene expression in Taniwaki, M. H., Hocking, A. D., Pitt, J. I., Fleet, G. H. (2009). Growth and Aspergillus flavus by temperature as revealed by RNA-Seq. FEMS Micro- mycotoxin production by food spoilage fungi under high carbon dioxide biology Letters, 322: 145–149. and low oxygen atmospheres. International Journal of Food Microbiology, Zhang, F., et al. (2014). RNA-Seq-based transcriptome analysis of aflatoxigenic 132: 100–108. Aspergillus flavus in response to water activity. 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Recent progress of the effect of environmental factors on Aspergillus flavus growth and aflatoxins production on foods

Tai,, Bowen; Chang,, Jinghua; Liu,, Yang; Xing,, Fuguo
Food Quality and Safety , Volume Advance Article – May 11, 2020
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© The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press.
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Abstract

The contamination of Aspergillus flavus and subsequent aflatoxins (AFs) has been considered as one of the most serious food safety problems due to their acute and chronic adverse effects on humans and animals. This review collects the available information from recent years on the effect of the major environmental factors such as water activity (a ), temperature, CO , and pH on the w 2 fungal growth, the expression of AFs-related genes, and AFs production by A. flavus on foods. In particular, the relationship between the relative expression of key regulatory (aflR and aflS) and structural genes (aflD, aflO, aflQ, etc.) and AFs production under different environmental conditions are collected and discussed. The information collected in this review can be used to design control strategies of A.  flavus and AFs contamination in practical applications, primarily during storage and processing. These data suggest that integrating various post-harvest methods with synergistic functions may be more efficient for the control of A. flavus growth and AFs production, although the individual environmental factors alone have an impact. Key words: Aspergillus flavus; aflatoxin; water activity; temperature; CO . growth retardation in children (Groopman et  al., 2008). Among Introduction AFs, aflatoxin B (AFB ) was the most toxic one. The main source 1 1 The moldy contamination of staple foods such as cereals has been of exposure to AFs is the ingestion of contaminated food and feed. regarded as one of the most serious food safety problems due to Therefore, the high threat of AFs to the health of humans and ani- their acute and chronic negative effects on humans and animals mals has resulted in strict legislative limits in most countries and (Medina et al., 2014). Certain molds such as Aspergillus flavus and regions of the world for AFs and AFB in a wide range of foodstuffs Aspergillus parasiticus grown in corn, peanuts, and nuts produce af- and feeds (Commission of the European Communities, 2010; US latoxins (AFs). AFs have been classified as carcinogens in Group 1 Food and Drug Administration, 2010). by the International Agency for Research on Cancer (IARC, 1993, Aspergillus flavus is the predominant fungal species contamin- 2002). They are estimated to induce up to 28% of the total world- ating foodstuffs and feeds and producing AFs worldwide. It is also wide cases of hepatocellular carcinoma (HCC), the most common the main contaminant during the food storage since its ability to form of liver cancer (Liu et  al., 2012; Wu, 2014). Moreover, AFs produce AFs and its potential to persist as a pathogen and saprophyte also inevitably cause acute intoxication, immune suppression, and © The Author(s) 2020. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by- nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 2 B. T ai et al. in the food supply before and after harvest (Lahouar et  al., 2015). is aimed at reviewing the effects of the major environmental factors Aspergillus flavus is a xerophilic fungus that has developed physio- on fungal growth and AFs production by A. avus fl . Several studies logical mechanisms that adapt to environmental stress factors like have revealed the effect of environmental factors on fungal growth, low water activity (a ), allowing them to compete and often dom- genes expression, and AFs production. In order to avoid duplication inate other fungal communities (Nierman, 2008; Medina et  al., with that presented by Medina et al. (2014), studies that displayed 2015). The competitive advantage is because its metabolic plasticity the effects of environmental factors in the above-mentioned review allows it to produce a range of extracellular hydrolases, secondary are not thoroughly discussed. The following subsections describe the metabolites, and volatiles (Magan and Aldred, 2007). Therefore, studies published after 2014 and papers not presented in the afore- preventing and controlling the fungal growth and AFs production mentioned review. This review may provide the basic data for opti- by A. avus fl are essential and urgent to ensure the food safety and mizing the environmental conditions to control AFs contamination security in the world. on foodstuffs and feeds, especially during the storage. To eliminate AFs contamination in food chain, the most useful and cost-effective strategy is to create an adverse environment for Effect of a and temperature on A. flavus growth, A.  avus fl growth and AFs production. The growth of A.  avus fl gene expression, and AFs production on grains at the phenotypic level and the AFs production were observed to be associated with several environmental factors such as a , tem- Plenty of literatures have reported that the two key environmental perature, storage time, composition of the substrate, carbon and parameters, a and temperature, play important roles in modulating nitrogen source, pH, light, content of oxygen (O ) and carbon di- the A. avus fl growth and AFs production on foods (O’Brian et  al., oxide (CO ), loss of grains’ integrity caused by insects or mechan- 2007; Schmidt-Heydt et al., 2009, 2010; Yu et al., 2011; Marroquín- ical/thermal damage, and the interaction between fungal species Cardona et al., 2014; Bai et al., 2015). Among foods, grains are the that share the same ecological environment (Dantigny et al., 2005; most susceptible to the infection of A.  avus fl and the subsequent Vaamonde et al., 2006; Astoreca et al., 2014; Medina et al., 2015). AFs contamination (Guo et  al., 1998). Regarding AFs production, Regarding abiotic factors, a and temperature and their interactions various grains have a different sensitivity to a and temperature. w w have been demonstrated to be the major aetiological determinants Moreover, on the same grain, the optimal conditions for AFs produc- in regulating fungal growth and secondary metabolites production tion were significantly influenced by the A. avus fl strains, incubation (Mannaa and Kim, 2017; Medina et al., 2017). As an aerobic fungus, time and status of grains, etc. A.  avus fl growth and subsequent AFs production are highly influ- Mannaa and Kim (2018) investigated the effects of different rela- enced by CO with certain levels (Peleg et  al., 1988; Mousa et  al., tive humidities (RHs; 12, 44, 76, and 98%) and temperatures (10, 20, 2016). AFs are biosynthesized by 29 genes located in a 75 Kb gene 30, and 40°C) on major grain fungal populations including A. avus fl cluster in A.  avus fl , including the two regulatory genes (aflS and and some other fungi. They indicated that the populations of all aflR) and the structural genes such as aflD, aflM, and aflO (Liu et al., tested fungi in inoculated rice grains were significantly enhanced by 2017). The biosynthesis of AFs is also regulated by genes encoding both increased RH and temperature. In addition, multiple linear re- the velvet proteins such as veA and laeA, as well as developmental gression analysis revealed that one unit increase of temperature re- genes modulating morphology, conidiation, or sclerotia formation sulted in greater effects than that of RH on fungal populations. like brlA and abaA (Caceres et  al., 2016). Some oxidative stress- Mousa et al. (2013) conducted a study to model the radial growth related genes and cellular signal mediator genes such as rasA, msnA, rate and to assess AFs production by A.  avus fl as a function of a mtfA, and oxylipin’s biosynthetic genes (Tsitsigiannis and Keller, 0.82–0.92 and temperature 12 –42°C on polished and brown rice. 2007); G-protein receptor genes (Affeldt et al., 2014); and osmotic- They found that the brown rice is more susceptible to fungal inva- adaptation response gene sakA (Tumukunde et  al., 2019) can also sion and AFs production than polished rice. The optimum conditions influence AFs biosynthesis (Caceres et al., 2016). for A. avus fl growth and AFs production in brown rice were both at The expression of AF pathway genes is also influenced by some 0.92 a and 30°C. Fungal growth and AFs were undetectable at 0.82 environmental factors. In particular, the a × temperature interactions a on polished rice while they were both detected at this a under w w w are related to the ratio of the two key regulatory genes (aflS/aflR). 25–35°C on brown rice. At the temperature range of 25–30°C, the And the higher ratio of aflS/aflR would relate to the higher level minimum a values for AFs production on polished rice and brown of AFs production (Schmidt-Heydt et  al., 2009, 2010; Abdel-Hadi rice were 0.84 and 0.82, respectively. The highest levels of AFs were et  al., 2010, 2012; Medina et  al., 2014). Tumukunde et  al. (2019) observed at the highest a 0.90–0.92 at 20°C after 21 days of incu- indicated that low a was negatively related to the production of bation on both types of rice. However, at 7 and 14 days of incuba- AFB on corn and peanut kernels. Low a reduced the expression tion, the highest level of AFs was observed at a 0.92 and 30°C on 1 w w of AfsakA, which affected the conidiation and AFs biosynthesis. polished rice. On brown rice, the optimal condition for AFs pro- Moreover, the expression of 11 development-related genes increased duction at 7 and 14 days of incubation was a 0.92 × 25°C and a w w under 0.99 a treatment (Zhang et al., 2014). As for high tempera- 0.92 × 30°C, respectively. When temperature reached to 40°C, only ture, aflS and aflR were inhibited. The expression level of aflS/aflR a small amount of AFs were detected during the 3 weeks of incuba- seems to control the transcriptional activation of the AFs cluster (Yu tion, and both types of rice were only detectable at 0.92 a . et al., 2011). Compared with 37°C, the transcript abundance of 30 Similarly, Choi et al. (2015) showed that brown Korean rice was AFs biosynthesis genes was much higher at 30°C, and most genes sensitive to A.  avus fl growth and AF production compared with were up-regulated at both protein and transcription levels at 28°C rough Korean rice and white Korean rice. Regardless of the degree (Bai et  al., 2015). Taken together, the environmental factors have of milling of Korean rice, the optimum growth rate during 120 day significant effects on A. avus fl growth, the expression of AF biosyn- storage was at 85% RH/30°C and 97% RH/21°C. The highest thetic genes, and AFs production. population of A. avus fl and highest amount of AFB were observed Therefore, controlling the environmental factors is the most at 97% RH/21°C and on inoculated brown rice. Trace amounts of useful, cost-effective, practical, and green environmental strategy to AFB were detected during 10 day storage at 85% RH/21°C and in prevent and eliminate A. avus fl and AF contaminations. This paper all three non-inoculated types of rice. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 3 Lv et al. (2019) investigated the effect of a (0.92–0.96) and tem- Effect of a and temperature on A. flavus growth, perature (28–37°C) on the fungal growth and AFB production by gene expression, and AFs production on peanuts A. avus fl on polished rice and paddy. The results indicated that AFB 1 Peanut (Arachis hypogaea L.) is a globally important economic and production on polished rice can occur over a wider range of tem- oilseed crop worldwide. However, peanuts contamination with AFs perature × a levels than that on paddies. Aspergillus avus fl grew w and aflatoxigenic A. avus fl is regarded as the most serious problem better at 0.92–0.96 a and 28–37°C on polished rice, and the highest w in the world (Williams et  al., 2004; Liu et  al., 2017). Liu et  al. level of AFB was observed at 33°C and 0.96 a after 7 days of incu- 1 w (2017) investigated the effect of a (0.85–0.99) and temperature bation. In comparison to the optimal temperature of 33°C, all tested (15–42°C) on fungal growth, the expression of AF biosynthetic genes of A.  avus fl on polished rice were significantly up-regulated genes on un-autoclaved peanut kernels. The results indicated that at 25°C under 0.96 a . Compared with a 0.96, most of structural w w AFB production in peanut kernels can occur over a wider range genes of pathway were significantly down-regulated at a 0.90 and w of a and temperature compared with formula media and peanut 0.99 under 33°C, although two regulatory genes (aflR and aflS) media. Aspergillus flavus showed a lower growth rate at ≤0.85 a were up-regulated at a 0.90. For the A. avus fl growth on paddy, the w or ≤20°C. The optimal conditions for A. avus fl growth on peanuts optimal temperature and a were 37°C and 0.94 within the tested w kernels were 0.98 a and 37°C. The highest amount of AFB was w 1 range, respectively. Moreover, the highest concentration of AFB on 1 observed at 0.96 a and 28°C. paddy was observed at 0.92 a and 37°C after 7 days of incubation. w Moreover, the expression of AF-related and growth-related genes Lahouar et al. (2016) evaluated the impact of a (between 0.85 w was significantly modulated by a and temperature. At 0.92 a , 16 w w and 0.99), temperature (15, 25, and 37°C), and incubation time of the 25 genes had the highest expression levels at 28°C, whereas 9 (7, 14, 21, and 28 days) on A. avus fl growth and AFB production 1 genes had the highest expression levels at 37°C. In addition, all AF by three A.  avus fl isolates (8, 10, and 14)  inoculated on sorghum biosynthetic pathway genes were down-regulated at 42°C compared grains. Results showed that the optimal conditions for growth and with 37°C. Compared with 0.99 a , all the pathway genes and laeA AFB production were at 0.99 a and 37°C. For mycelial growth, the 1 w were up-expressed at a of 0.96 under 28°C. In particular, the ratio needed minimum a was 0.91 at 25 and 37°C. AFB accumulation w 1 of aflS/aflR was positively correlated with the AFB production. The could be avoided by storing sorghum at low a levels (≤0.91 a ) or w w expressions of laeA and brlA were positively associated with AFB at low temperature (15°C). production and fungal growth, respectively. Astoreca et al. (2014) studied the interaction of a (0.80–0.98), temperature (10–40°C), and incubation time (7, 14, 21, and 28 days) Effect of a and temperature on A. flavus growth on the co-production of AFB and cyclopiazonic acid (CPA) by and AFs production on tree nuts A. avus fl isolated from corn on Czapek yeast agar (CYA) and corn extract agar (CEM). They found the AFB production occurred more Tree nuts are commodities with moderate to high risk of AFs con- favourably on CYA while the maximum levels of CPA were observed tamination because they are produced at environmental conditions on CEM. The minimum level of a for both toxins production was favouring fungal growth and AFs production by aflatoxigenic fungi 0.83 with the tested a . The maximum amount of AFB was ob- especially A. avus fl (Arrus et  al., 2005; Gallo et  al., 2016). The in- w 1 served at 0.96 a and 30°C after 21 days of incubation, regardless cidence of AFs contamination in nuts is low; however, their levels of the isolates and media. Although they belong to three different vary widely and can produce high levels in a small number of nuts chemotypes: chemotype I  (AFB +/CPA+), chemotype III (AFB +/ (Campbell et al., 2003). 1 1 CPA−), and chemotype IV (AFB −/CPA+), respectively, the three iso- For the pistachio nuts, the highest amount of radial growth rate lates do not differ in the response to the environmental factors (a of A. avus fl and AFB production was obtained at 0.93 a and 30°C w 1 w and temperature). Moreover, the limiting and optimum conditions using a full factorial design with different moisture content levels for AFB and CPA production were similar on both media. (10, 15, 20, 25, and 30%) and incubation temperatures (10, 15, 20, Bernáldez et al. (2017) investigated the impact that interactions 25, 30, 37, and 42°C) (Marín et al., 2012). They also found that the between a and temperature may have on growth, the expression of limited AFs levels in pistachio nuts by European Commission would aflR, and AFB production by A. avus fl on a maize-based medium. be surpassed in a period as short as 1 month if pistachio nuts reach They found that there were some differences between lag phases 20°C, unless moisture content is ≤10%. However, this conclusion and growth rates of A. avus fl . The optimum condition for A. avus fl is not accurate because it was drawn from a single A. avus fl strain. growth on maize was 0.99 a and 30°C and the maximum AFB As we all know, the level of mycotoxins produced is highly variable w 1 production on maize was observed at 0.98 a and 30°C. Aspergillus even if only considering mycotoxin-producing strains in a species avus fl growth was completely inhibited at 0.90 a and 20°C. Both (Hua et al., 2012). a and temperature significantly influenced the relative expression Gallo et  al. (2016) evaluated the effects of different combin- of aflR gene and AFB production. However, the influences on AFB ations of a (0.90, 0.93, 0.96, and 0.99 a ) and temperature (20, 28, 1 1 w w production were not consistent with the effects on gene expression and 37°C) on A.  avus fl growth, AFB production, and expression and growth. These results suggested that the aflR expression was not of the two regulatory genes and two structural genes on an almond a good indicator of AFB production alone. Therefore, further mo- medium solidified with agar. The maximum amount of fungal bio- lecular studies of other AFs biosynthetic genes should be conducted. mass and AFB production was observed at 0.96 a and 28°C. At 1 w Based on the research by Krulj et  al., (2019), the optimal con- the driest tested conditions (0.90 and 0.93 a ), no fungal growth ditions for AFB biosynthesis were observed at 30°C in the tem- and AFB production were observed at 20°C. At 20 and 37°C, the 1 1 perature ranges of 15–37°C and the a levels at (0.85–0.99) in the yield of AFB was reduced by 70%–90% or completely suppressed, w 1 inoculated shell-less and shelled cereals. Moreover, the shell has a depending on a . Both regulatory genes (aflR and aflS) showed high higher amount of AFB in hull-less grain than the dehulled grains expression at maximum (28°C) and minimal (20 and 37°C) AFB 1 1 and the AFB content in the hull was even 10–170 times higher than production. In contrast, the two structural genes (aflD and aflO) the grain, indicating the shell has a protective effect. showed high expression only at the maximum AFB production 1 Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 4 B. T ai et al. (28°C and 0.96–0.99 a ). Based on this, temperature appears to be temperature. Regarding A.  parasiticus, the highest and lowest ex- a key factor affecting AFs production, which was strictly correlated pression values of both regulatory genes were observed at 0.95 a with the expression of the structural genes (aflD and aflO), but not and 0.85 a , respectively. In contrast, the expression of aflP gene in to that of the two regulatory genes. This result suggests that some both species was stimulated at low temperature and a . Furthermore, post-transcriptional regulatory processes are involved in modulating a strong correlation between the relative expression of aflR and aflS AFs biosynthesis. gene and AFs production was obtained under environmental condi- Prencipe et al. (2018) evaluated the drying temperatures (from 30 tions which simulate dry-cured ham ripening. to 50°C) on A. avus fl growth and AFs production in chestnuts and indicated that the optimal temperature for fungal growth was 30°C, Effect of other environmental factors on A. flavus whereas the highest concentrations of AFB and AFB were obtained 1 2 growth and AFs production on food at 40°C. At this temperature, A. avus fl was under suboptimal condi- In addition to a and temperature, there are more environmental tions for growth (0.78 a ), but AFs biosynthesis was under the op- parameters that have been investigated for the influences on the timal conditions. When the drying temperatures reached 45–50°C, growth and AFs production by A. avus fl in many studies. It has been AFs production was completely inhibited. Drying at 45°C for 7 days reported that pH, CO level, and light treatment also exhibit signifi- (0.64 a ) could be a promising strategy to effectively control both cant effects on fungal growth and AFs production (Schmidt-Heydt A. flavus growth and AFs production. et al., 2008; Oms-Oliu et al., 2010; Castellari et al., 2015). Regarding pH, Casquete et  al. (2017) investigated the effect of Effect of a and temperature on A. flavus pH (5.0, 5.5, and 6.0), a (0.90, 0.95, and 0.99), and temperature growth, gene expression, and AFs production on (15, 20, 25, and 30°C) on the lag phases, growth, and AFs produc- other foods tion of three aflatoxigenic A. avus fl strains (CQ7, CQ8, and CG103) on cheese-based medium. The results showed that the behaviour of Recently, there are some researches that reported the effect of a and A. avus fl strains was affected by pH, a , and temperature; however, temperature on the fungal growth and AFs production by A. avus fl A. avus fl growth was less affected by pH than the others. The CQ7 on other foods. In whole black peppercorns (Piper nigrum L.), the strain exhibited maximum growth at pH 5.5, 0.99 a , and 25°C. growth and AFs production of three A.  avus fl isolates and one However, for the CQ8 and CQ103 strains, there was no difference A.  parasiticus isolate were investigated using a full factorial design between pH 5.5 and 6.0. The maximum AFs production on the with seven a levels (0.826–0.984) and three temperatures (22, 30, cheese-based medium occurred at pH 5.0, 0.95 a , and 25 or 30°C, and 37°C) (Yogendrarajah et al., 2016). Among secondary models, depending on the strain. Kosegarten et al. (2017) also indicated that the extended Gibson model was the best model to describe the com- an increase in pH value between 3.5 and 6.5 resulted in an increase bined effect of a and temperature on the growth rate of both fungal in the growth of A. flavus. species in peppercorns. The highest population of A. avus fl occurred For CO level, Mousa et  al. (2016) illustrated that the growth at 0.92 a and 30°C, and the maximum yield of AFB was also ob- w 1 of A. avus fl and AFs production was highly influenced by the CO served under this condition based on diverse secondary models. The level (20%–80%) on paddy. In general, fungal growth rates and estimated minimum a and temperature for the growth of A. avus fl AFs production were negatively correlated with CO , whereas the were 0.73–0.76 and 11–16°C, respectively. High variability in AFs lag phase durations were positively correlated with CO . However, production of different aflatoxigenic species limited the modelling the highest tested CO level (80%) could not completely inhibit the of AFs production. Based on the research of Yogendrarajah et  al. fungi growth. Under 0.98 a , 20% and 80% CO caused at least (2016), the limiting a and temperature should be considered to pre- w 2 59% and 88% reduction in growth and 47% and 97% reduction vent the aflatoxigenic fungal species growth and AFs production in in AFs production, respectively. In addition, a significant inhibition food during storage. of growth was observed at 75% CO at both 0.95 and 0.92 a on Peromingo et  al. (2016) evaluated that the interaction between 2 w agar medium. The population of A. avus fl isolated from grains was a (0.85, 0.90, and 0.95) and temperature (10, 15, 20, and 25°C) inhibited at up to 75% CO (Giorni et al., 2008). Giorni et al. (2008) may occur on lag phases prior to growth, growth rates, and AFs also has reported that the moisture maize treated with 25% CO was production by two strains of each A.  parasiticus and A.  avus fl on sufficient to effectively reduce the development of A. avus fl , but at cured meat over 12 days. Aspergillus flavus CBS 573.65 had shorter least 50% CO was required to significantly reduce the synthesis of lag phases than A.  parasiticus CECT 2 688; however, the growth AFs. Therefore, controlling pH and CO levels during manufacturing rates of the two strains were similar. The optimum growth and AFs and storage is an effective control strategy to avoid the contamin- production occurred at 0.95 a and 25°C. At 10°C and all tested ation of A. flavus and subsequent AFs (Chulze, 2010). a , no growth occurred for both species. Both species produced AFs when the a and temperature were a ≥ 0.90 and ≥15°C, respect- w w ively. Although similar AFB production characteristics were found Discussion and Conclusions between the two species, the concentration of this toxin produced by A. flavus was much higher than that of A. parasiticus. These previous studies have indicated that several environmental To elucidate the relationship between the relative expression factors play important roles in regulating fungal growth, the expres- of AFs-related genes and AFs production, Peromingo et  al. (2017) sion of AF biosynthetic genes, and AFs production by A. avus fl and evaluated the effect of different a and temperatures on the temporal A.  parasiticus. Especially, a and temperature are limiting factors w w relative expression of three genes in AFs biosynthesis cluster and during storage (Liu et al., 2017). Therefore, this review summarizes their correlation with AFs production on dry-cured ham-based me- the different ranges of a and temperature and the optimal condition dium by A. avus fl and A. parasiticus. In general, the expressions of for A. avus fl growth and AFs production on different food substrate the regulatory aflR and aflS genes were similar and much lower than and formula media (Figures 1 and 2). As shown in the two figures, the expression of the structural aflP gene. The expression of aflR and the optimal conditions of a × temperature for A.  avus fl growth aflS genes in A. avus fl increased over a decrease of a regardless of and AFs production vary on different foods or formula medium (Lv w Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 5 Figure 1. Comparison of a and temperature ranges and the optimal Figure 2. Comparison of a and temperature ranges and the optimal conditions (the black line) for the growth of A.  flavus in different food conditions (the black line) for the aflatoxin (AF) production in different food matrices and formula medium. (A) Aspergillus flavus growth at different a . matrices and formula medium. (A) AF production at different a . (B) AF (B) Aspergillus flavus growth at different temperatures. production at different temperatures. aflS were highlighted. On YES medium, the down-regulation of aflR et  al., 2019). On yeast extract sucrose (YES) medium, the suitable and aflS induced the inhibition of AFs production (Yu et al., 2011). temperatures for AFB production were 25–30°C at 0.99 a , whereas 1 w And the decrease in the expression ratio of aflS/aflR leads to tran- the range changed to 30–35°C at 0.95 a (Abdel-Hadi et al., 2012). scription inactivation of AFs cluster. Similar findings were obtained On un-autoclaved peanut kernels, the suitable temperatures for on un-autoclaved peanut kernels (Liu et  al., 2017). At 42°C, the AFB production were 0.92–0.96 a and 25–33°C, and the highest 1 w lower ratio of aflS/aflR resulted in lower AFB production compared level of AFB was observed at 0.96 a and 28°C (Liu et al., 2017). 1 w 1 with 28 and 37°C. Similar findings were obtained on almond medium; the maximum In contrast, some literatures have reported that the aflR expres- fungal growth and AFB production were observed at 0.96 a and 1 w sion is not consistent with AFs production at several conditions. 28°C (Gallo et al., 2016). On un-autoclaved polished rice, high pro- On a maize-based medium, the influences of a and temperature duction of AFB was observed at 0.90–0.99 a and 25–33°C, and the 1 w w on AFB production were different with the expression of aflR gene maximum amount of AFB was obtained at 0.96 a and 33°C (Lv 1 w 1 (Bernáldez et al., 2017). On polished rice, the down-regulation of all et al., 2019). Moreover, these results suggest that the fungal growth the tested AFs structural genes at a 0.90 resulted in a low level of and AFs production on foods can occur over a wider range of a × w w AFB production compared with a 0.96, although aflR and aflS were temperature than on formula medium. The diversity of optimal con- 1 w both up-regulated (Lv et  al., 2019). Similar findings were reported ditions may be due to the differences in media structure and nutrient by O’Brian et al. (2007), who obtained an opposite relationship be- availability (Ahmad et al., 2013; Mousa et al., 2013). tween AFs biosynthesis and the expression of aflR and aflS. AFs pro- Compared with the investigations published before 2015, the re- duction was completely inhibited at 37°C although both regulatory cent publications pay more attention to the correlation between the genes were highly expression in liquid A  and M media. Schmidt- expression of AFs biosynthetic genes and AFs production. The re- Heydt et al. (2009) indicated that the transcription level of aflS was searchers attempt to get a good indicator of possible AFs contamin- high at >37°C under almost all a ranges tested, but the amount ation on foods by early detecting the expression of AFs-related genes. of AFs production was low on YES medium. These results suggest As the key regulatory genes in AFs biosynthesis gene cluster, aflR and Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 6 B. T ai et al. that some other molecular mechanisms, such as post-transcriptional 2008). It is important to notice that the residual O may be a limiting mechanism, were involved in modulating the transcriptional level of factor for fungal growth and AFs production under modified atmos- AFs structural genes and the subsequent AFs production. phere packaging (Taniwaki et al., 2009). Compared with the two regulatory genes aflR and aflS, the tran- The pH is also an important factor in determining A.  avus fl scriptional levels of some structural genes seem to have more strong growth and AFs production. Klich (2007) indicated that the increase correlation to AFs production. Gallo et al. (2016) indicated that the in pH (4–6) was related to the increase of A. avus fl growth, and the effect of environmental factors on AFs biosynthesis had a better expression of the AFs pathway gene was also affected by the pH of correlation to the transcriptional activation/inactivation of struc- the medium. In some foods such as fermented food, salted food, and tural genes (aflD and aflO) than the two regulatory genes. Similarly, canned food, fungal growth and AFs production can be controlled Abdel-Hadi et al. (2010) also obtained a good correlation between by adjusting pH values. However, there are some limitations on the aflD expression and AFB production by A.  avus fl in raw peanuts practical application of adjusting pH in most foods, especially the under different a levels. In addition, the significant differences be- grains and spices listed in this paper. tween the relative expression of aflD at different temperatures (28, In conclusion, the low a and temperature or the increase in the 37, and 42°C) were observed, resulting in the significant differences CO level alone is not effective for complete control of A.  avus fl in AFB production on peanut kernels (Liu et  al., 2017). On YES and AFs production. Integrating various post-harvest methods with medium, the expression profile of aflD, aflO, and aflP was consist- synergistic functions may be more efficient for the complete inhib- ently correlated with the ability of AFs production (Scherm et  al., ition of A.  avus fl growth and AFs production during storage and 2005). On polished rice, the structural genes (aflM, aflN, aflO, aflP, processing of foods. For example, reducing a is the prerequisite aflQ, aflU, and nadA) involved in the middle and late stages of AFs step to prevent A.  avus fl infection and AFs production, and con- pathway from VERA (Versicolorin A) to AFB were down-regulated trolling a and temperature and increasing the level of CO in the 1 w 2 at 37°C compared with 33°C under a 0.96 (Lv et  al., 2019). The atmosphere are useful strategies during storage. Good Agricultural lower expression of these structural genes led to the decrease of AFB Practices (GAP) and Good Processing Practices (GPP) represent pri- production. On peanuts kernels, a good positive correlation between mary preventive measures against A. avus fl and the subsequent AFs. the expression of aflQ, being involved in the final step of the AFs Integrating the two principles with the Hazard Analysis and Critical biosynthetic pathway and encoding an oxidoreductase, and AFB Control Point (HACCP) can be used efficiently (Mousa et al., 2016). level was observed under different a ’s and temperatures (Liu et al., A  better knowledge of the environmental factors governing fungal 2017). Taken together, these results suggest that an early detection of growth and AFs production provided in the above-mentioned recent the expression of some key structural genes (aflD, aflO, aflP, or aflQ) researches would help in establishing optimal guidelines in GAP and can be a better indicator of possible AFs contamination on foods GPP, preventive measures, and critical limits in HACCP plans. under different a ’s and temperatures compared with aflS and aflR. Besides modulating a and temperature, modified atmosphere Acknowledgements packaging is regarded as a promising food preservation technique because it integrates the control microbial activity and insects, which We gratefully acknowledge the financial support of National Key R&D tend to maintain the quality of the products and extend the shelf life Program of China (2016YFD0400105). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the with minimal application of chemicals (Taniwaki et al., 2009; Mousa manuscript. et al., 2016). CO was proved to retard the fungal growth and inhibit AFs production by A. avus fl . Taniwaki et  al. (2009) indicated that no fungal growth of A. avus fl was observed at 40% and 60% CO Conflict of Interest when O level was <0.5% while growth was observed on PDA and None declared. CYA at 20% CO . However, even at the lowest CO level (20%) 2 2 studied, the retarding effect of CO on the growth rate of A. avus fl was significant on paddy (Mousa et al., 2016). Overall, 55%–100% References reduction in fungal growth was achieved with CO treatment. On Abdel-Hadi,  A., Carter,  D., Magan,  N. (2010). Temporal monitoring of the moistened maize, modified atmospheres with 25%–50% CO only nor-1 (aflD) gene of Aspergillus flavus in relation to aflatoxin B produc- contributed to 30%–35% reduction in A. avus fl growth while as the tion during storage of peanuts under different water activity levels. Journal concentrations of CO increased up to 75%, the reduction of above of Applied Microbiology, 109: 1914–1922. 50% was obtained (Giorni et  al., 2008). The more reduction of Abdel-Hadi, A., Schmidt-Heydt, M., Parra, R., Geisen, R., Magan, N. (2012). fungal growth on paddy than maize with CO treatment may be due A systems approach to model the relationship between aflatoxin gene to the more resistance of paddy’s physical structure to the invading cluster expression, environmental factors, growth and toxin production fungi (Mousa et al., 2016). by Aspergillus flavus. Journal of the Royal Society, Interface, 9: 757–767. Besides fungal growth, AFs production was also significantly Affeldt, K. J., Carrig, J., Amare, M., Keller, N. P. (2014). Global survey of ca- inhibited by modified atmosphere with CO . Mousa et  al. (2016) nonical Aspergillus flavus G protein-coupled receptors. Mbio, 5: e01501– e01514. found that the reduction in AFs production on paddy with CO Ahmad, M., Ahmad, M. M., Hamid, R., Abdin, M. Z., Javed, S. (2013). Use of treatment (20%–80%) was in the range of 65.8%–98.0%, 70.4%– response surface methodology to study the effect of media composition on 94.6%, and 72.9%–96.8% at 0.98, 0.95, and 0.92 a , respectively. aflatoxin production by Aspergillus flavus. Mycotoxin Research, 29: 39–45. However, no significant reduction in AFs production on maize was Arrus, K., Blank, G., Abramson, D., Clear, R., Holley, R. A. (2005). Aflatoxin observed with modified atmosphere enriched with 25% CO and production by Aspergillus flavus in Brazil nuts. Journal Stored Products balanced with N (Giorni et al., 2008). With the application of 50% Research, 41(5): 513–527. and 75% CO , 46% and 58% overall reduction in AFs production Astoreca, A., Vaamonde, G., Dalcero, A., Marin, S., Ramos, A. (2014). Abiotic was observed, respectively. Additionally, on PDA or CYA enclosed factors and their interactions influence on the co-production of aflatoxin with a modified atmosphere with 20% CO and <0.5% residual B(1) and cyclopiazonic acid by Aspergillus avus fl isolated from corn. Food oxygen, no AFs production was observed for 30 days (Giorni et al., Microbiology, 38: 276–283. Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 The effect of environmental factors on Aspergillus flavus 7 Bai, Y., et al. (2015). Integrative analyses reveal transcriptome-proteome cor- Krulj, J., et al. (2019). The effect of storage temperature and water activity on relation in biological pathways and secondary metabolism clusters in aflatoxin B1 accumulation in hull-less and hulled spelt grains. Journal of A. flavus in response to temperature. Scientific Reports, 5: 14582. the Science of Food and Agriculture, 99: 3703–3710. Bernáldez, V., Córdoba, J. J., Magan, N., Peromingo, B., Rodríguez, A. (2017). Lahouar, A., Crespo-Sempere, A., Marín, S., Saïd, S., Sanchis, V. (2015). Toxi- The influence of ecophysiological factors on growth, aflR, gene expression genic molds in Tunisian and Egyptian sorghum for human consumption. and aflatoxin B1 production by a type strain of Aspergillus flavus. LWT - Journal of Stored Products Research, 63: 57–62. Food Science and Technology, 83: 283–291. Lahouar, A., Marin, S., Crespo-Sempere, A., Saïd, S., Sanchis, V. (2016). Ef- Caceres,  I., et  al. (2016). Deciphering the anti-aflatoxinogenic properties of fects of temperature, water activity and incubation time on fungal growth eugenol using a large-scale q-PCR approach. Toxins, 8: 123. and aflatoxin B1 production by toxinogenic Aspergillus flavus isolates on Campbell, B. C., Molyneux, R. J., Schatzki, T. F. (2003). Current research on sorghum seeds. Revista Argentina De Microbiologia, 48: 78–85. reducing pre‐ and post‐harvest aflatoxin contamination of U.S.  almond, Liu, Y., Chang, C. C., Marsh, G. M., Wu, F. (2012). Population attributable pistachio, and walnut. Toxin Reviews, 22(2–3): 225–266. risk of aflatoxin-related liver cancer: systematic review and meta-analysis. Casquete,  R., Benito,  M.  J., Córdoba,  M.  G., Ruiz-Moyano,  S., Martín,  A. European Journal of Cancer (Oxford, England: 1990), 48: 2125–2136. (2017). The growth and aflatoxin production of Aspergillus flavus strains Liu, X., Guan, X., Xing, F., Lv, C., Dai, X., Liu, Y. (2017). Effect of water ac- on a cheese model system are influenced by physicochemical factors. tivity and temperature on the growth of Aspergillus flavus, the expression Journal of Dairy Science, 100: 6987–6996. of aflatoxin biosynthetic genes and aflatoxin production in shelled pea- Castellari, C. C., Cendoya, M. G., Marcos Valle, F. J., Barrera, V., Pacin, A. M. nuts. Food Control, 82: 325–332. (2015). [Extrinsic and intrinsic factors associated with mycotoxigenic Lv,  C., et  al. (2019). Interaction of water activity and temperature on the fungi populations of maize grains (Zea mays L.) stored in silobags in Ar- growth, gene expression and aflatoxin production by Aspergillus flavus on gentina]. Revista Argentina De Microbiologia, 47: 350–359. paddy and polished rice. Food Chemistry, 293: 472–478. Choi,  S., et  al. (2015). Behaviour of Aspergillus flavus and Fusarium Magan,  N., Aldred,  D. (2007). Post-harvest control strategies: minimizing graminearum on rice as affected by degree of milling, temperature, and mycotoxins in the food chain. International Journal of Food Microbiology, relative humidity during storage. Food Microbiology, 46: 307–313. 119: 131–139. Chulze,  S.  N. (2010). Strategies to reduce mycotoxin levels in maize during Mannaa, M., Kim, K. D. (2017). Influence of temperature and water activity storage: a review. Food Additives & Contaminants. Part A, Chemistry, on deleterious fungi and mycotoxin production during grain storage. Analysis, Control, Exposure & Risk Assessment, 27: 651–657. Mycobiology, 45: 240–254. Commission of the European Communities. (2010). Commission regulation Mannaa, M., Kim, K. D. (2018). Effect of temperature and relative humidity (EU) No 165/2010 of 26 February 2010 amending Regulation (EC) No on growth of Aspergillus and Penicillium spp. and biocontrol activity of 1881/2006 setting maximum levels for certain contaminants in foodstuffs Pseudomonas protegens AS15 against aflatoxigenic Aspergillus flavus in as regards aflatoxins. Official Journal of European Union, 50: 8–12. stored rice grains. Mycobiology, 46: 287–295. Dantigny, P., Guilmart, A., Radoi, F., Bensoussan, M., Zwietering, M. (2005). Marín,  S., Ramos,  A.  J., Sanchis,  V. (2012). Modelling Aspergillus flavus Modelling the effect of ethanol on growth rate of food spoilage moulds. growth and aflatoxins production in pistachio nuts. Food Microbiology, International Journal of Food Microbiology, 98: 261–269. 32: 378–388. Gallo, A., Solfrizzo, M., Epifani, F., Panzarini, G., Perrone, G. (2016). Effect Marroquín-Cardona,  A.  G., Johnson,  N.  M., Phillips,  T.  D., Hayes,  A.  W. of temperature and water activity on gene expression and aflatoxin bio- (2014). Mycotoxins in a changing global environment–a review. Food and synthesis in Aspergillus flavus on almond medium. International Journal Chemical Toxicology, 69: 220–230. of Food Microbiology, 217: 162–169. Medina,  A., et  al. (2017). Interactions between water activity and tempera- Giorni,  P., Battilani,  P., Pietri,  A., Magan,  N. (2008). Effect of a and CO ture on the Aspergillus avus fl transcriptome and aflatoxin B1 production. w 2 level on Aspergillus avus fl growth and aflatoxin production in high mois- International Journal of Food Microbiology, 256: 36–44. ture maize post-harvest. International Journal of Food Microbiology, 122: Medina,  A., Rodriguez,  A., Magan,  N. (2014). Effect of climate change on 109–113. Aspergillus flavus and aflatoxin B1 production. Frontiers in Microbiology, Groopman, J. D., Kensler, T. W., Wild, C. P. (2008). Protective interventions to 5: 348. prevent aflatoxin-induced carcinogenesis in developing countries. Annual Medina,  A., Schmidt-Heydt,  M., Rodríguez,  A., Parra,  R., Geisen,  R., Review of Public Health, 29: 187–203. Magan,  N. (2015). Impacts of environmental stress on growth, sec- Guo,  B.  Z., Brown,  R.  L., Lax,  A.  R., Cleveland,  T.  E., Russin,  J.  S., ondary metabolite biosynthetic gene clusters and metabolite production Widstrom, N. W. (1998). Protein profiles and antifungal activities of kernel of xerotolerant/xerophilic fungi. Current Genetics, 61: 325–334. extracts from corn genotypes resistant and susceptible to Aspergillus Mousa,  W., Ghazali,  F.  M., Jinap,  S., Ghazali,  H.  M., Radu,  S. (2013). avus fl . Journal of Food Protection, 61: 98–102. Modeling growth rate and assessing aflatoxins production by Aspergillus Hua, S. S., McAlpin, C. E., Chang, P. K., Sarreal, S. B. (2012). Characteriza- avus fl as a function of water activity and temperature on polished and tion of aflatoxigenic and non-aflatoxigenic Aspergillus avus fl isolates from brown rice. Journal of Food Science, 78: M56–M63. pistachio. Mycotoxin Research, 28: 67–75. Mousa, W., Ghazali, F. M., Jinap, S., Ghazali, H. M., Radu, S., Salama, A. E. R. International Agency for Research on Cancer. (1993). Some naturally occurring (2016). Temperature, water activity and gas composition effects on the substances: food items and constituents, heterocyclic aromatic amines and growth and aflatoxin production by Aspergillus flavus on paddy. Journal mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risks of Stored Products Research, 67: 49–55. to Humans, 56: 245–395. Nierman,  W.  T. (2008). Mycotoxin production and prevention of aflatoxin International Agency for Research on Cancer. (2002). Some traditional herbal contamination in food and feed. Aspergilli Genomics Medical Aspects medicines, some mycotoxins, naphthalene and styrene. IARC Monographs Biotechnology & Research Methods, 8(8): 84–88. on the Evaluation of Carcinogenic Risks to Humans, 82: 1–556. O’Brian, G. R., et al. (2007). The effect of elevated temperature on gene tran- Klich,  M.  A. (2007). Environmental and developmental factors influencing scription and aflatoxin biosynthesis. Mycologia, 99: 232–239. aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Oms-Oliu,  G., Martín-Belloso,  O., Soliva-Fortuny,  R. (2010). Pulsed light Mycoscience, 48(2): 71–80. treatments for food preservation. A  review. Food and Bioprocess Tech- Kosegarten,  C.  E., Ramírez-Corona,  N., Mani-López,  E., Palou,  E., López- nology, 3(1): 13–23. Malo, A. (2017). Description of Aspergillus flavus growth under the influ- Peleg,  Y., Stieglitz,  B., Goldberg,  I. (1988). Malic acid accumulation by ence of different factors (water activity, incubation temperature, protein Aspergillus avus fl . Applied Microbiology and Biotechnology, 28(1): 69– and fat concentration, pH, and cinnamon essential oil concentration) by 75. kinetic, probability of growth, and time-to-detection models. International Peromingo,  B., Rodríguez,  A., Bernáldez,  V., Delgado,  J., Rodríguez,  M. Journal of Food Microbiology, 240: 115–123. (2016). Effect of temperature and water activity on growth and aflatoxin Downloaded from https://academic.oup.com/fqs/advance-article-abstract/doi/10.1093/fqsafe/fyz040/5763063 by guest on 03 March 2020 8 B. T ai et al. production by Aspergillus flavus and Aspergillus parasiticus on cured meat Tsitsigiannis,  D.  I., Keller,  N.  P. (2007). Oxylipins as developmental and model systems. Meat Science, 122: 76–83. host-fungal communication signals. Trends in Microbiology, 15: 109– Peromingo,  B., Rodríguez,  M., Delgado,  J., Andrade,  M.  J., Rodríguez,  A. 118. (2017). Gene expression as a good indicator of aflatoxin contamination in Tumukunde, E., Li, D., Qin, L., Li, Y., Shen, J. J., Wang, S. H., Yuan, J. (2019). dry-cured ham. Food Microbiology, 67: 31–40. Osmotic-adaptation response of sakA/hogA gene to aflatoxin biosyn- Prencipe,  S., Siciliano,  I., Gatti,  C., Gullino,  M., Garibaldi,  A., Spadaro,  D. thesis, morphology development and pathogenicity in Aspergillus avus fl . (2018). Chestnut drying is critical in determining Aspergillus flavus Toxins, 11: 41. growth and aflatoxin contamination. Toxins, 10(12): 530. US Food and Drug Administration (2010). Aflatoxin in Peanuts and Peanut Scherm, B., Palomba, M., Serra, D., Marcello, A., Migheli, Q. (2005). Detec- Products: 2010; CPG Sec. 570.375. Compliance Manuals. http://www.fda. tion of transcripts of the aflatoxin genes aflD, aflO, and aflP by reverse gov/ICECI/ComplianceManuals. Accessed 16 August 2019. transcription-polymerase chain reaction allows differentiation of aflatoxin- Vaamonde, G., Patriarca, A., Fernández Pinto, V. E. (2006). Effect of water ac- producing and non-producing isolates of Aspergillus flavus and Aspergillus tivity and temperature on production of aflatoxin and cyclopiazonic acid parasiticus. International Journal of Food Microbiology, 98: 201–210. by Aspergillus flavus in peanuts. Advances in Experimental Medicine and Schmidt-Heydt, M., Abdel-Hadi, A., Magan, N., Geisen, R. (2009). Complex Biology, 571: 225–235. regulation of the aflatoxin biosynthesis gene cluster of Aspergillus flavus in Williams, J. H., Phillips, T. D., Jolly, P. E., Stiles, J. K., Jolly, C. M., Aggarwal, D. relation to various combinations of water activity and temperature. Inter- (2004). Human aflatoxicosis in developing countries: a review of toxi- national Journal of Food Microbiology, 135: 231–237. cology, exposure, potential health consequences, and interventions. The Schmidt-Heydt, M., Magan, N., Geisen, R. (2008). Stress induction of myco- American Journal of Clinical Nutrition, 80: 1106–1122. toxin biosynthesis genes by abiotic factors. FEMS Microbiology Letters, Wu, F. (2014). Perspective: time to face the fungal threat. Nature, 516: S7. 284: 142–149. Yogendrarajah,  P., et  al. (2016). Mycotoxin production and predictive Schmidt-Heydt,  M., Rüfer,  C.  E., Abdel-Hadi,  A., Magan,  N., Geisen,  R. modelling kinetics on the growth of Aspergillus flavus and Aspergillus (2010). The production of aflatoxin B1 or G 1 by Aspergillus parasiticus parasiticus isolates in whole black peppercorns (Piper nigrum L). Inter- at various combinations of temperature and water activity is related to the national Journal of Food Microbiology, 228: 44–57. ratio of aflS to aflR expression. Mycotoxin Research, 26: 241–246. Yu, J., et al. (2011). Tight control of mycotoxin biosynthesis gene expression in Taniwaki, M. H., Hocking, A. D., Pitt, J. I., Fleet, G. H. (2009). Growth and Aspergillus flavus by temperature as revealed by RNA-Seq. FEMS Micro- mycotoxin production by food spoilage fungi under high carbon dioxide biology Letters, 322: 145–149. and low oxygen atmospheres. International Journal of Food Microbiology, Zhang, F., et al. (2014). RNA-Seq-based transcriptome analysis of aflatoxigenic 132: 100–108. Aspergillus flavus in response to water activity. Toxins, 6: 3187–3207.

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