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Purpose The purpose of this study was to isolate the surface-associated microorganisms from the dairy plant surfaces with a high probability of biofilm formation and determine the most adhesive strains in terms of surface properties and exopolysaccharide production. Methods Four hundred and ninety-five surface-associated microorganisms were isolated from potential biofilm-forming surfaces of a dairy plant. One hundred and seventy of these were isolated after cleaning/disinfection of the pasteurized milk, white cheese and butter tank, yogurt and ice cream filling unit, ice cream air pressing, and condensed milk pipe. It is noteworthy that some isolates might cause post-production contamination, food infection, and intoxication. Selected 42 isolates were identified by Gram staining, physiological and biochemical tests, and 16S rRNA gene sequencing. Then, surface properties and exopolysaccharide production of 10 selected isolates were determined. To evaluate the surface properties, microbial adhesion to hydrocarbons, static water contact angle, salt aggregation, and surface zeta potential tests were performed. Result The microbial adhesion to hydrocarbons (MATH) test exhibited the lowest standard deviations, and the most consistent results between the replicates. The highest hydrophilic characteristics and exopolysaccharide production were exhibited by Gram-negative Pseudomonas aeruginosa, followed by Gram-positive Bacillus toyonensis. Also, a significant diversity of neutral sugar was determined in their alditol acetate forms by using gas chromatography–mass spectrometry. In this context, it is believed that the determination of the EPS content of the isolates would contribute to establishing an effective cleaning/disinfection procedure for dairy plants. Conclusion This study indicated that microbial adhesion is still a common problem in the dairy industry. Because of this situation, dairy plants should be organized and constructed to be suitable for hygiene and sanitary applications. . . . . . Keywords Dairy plant Adhesion Identification Surface property Exopolysaccharide production Neutral sugar content Introduction living surfaces or irreversibly to each other. Microorganisms in biofilms have a different phenotype in terms of their repro- Biofilm is a microbial-derived cell community located in a ductive rate and gene transcription profile compared with matrix that contains extracellular polymeric substances, which planktonic types (Donlan and Costerton 2002). These micro- allows microorganisms to bind irreversibly to living and non- organisms are typically more virulent, more easily adaptable to changing environmental factors, and are able to develop resistance to antibiotics (Watnick and Kolter 2000). Numerous examples of the microorganisms are isolated * Dilay Kütük Ayhan dilaykutuk@hacettepe.edu.tr from dairy plants in literature (Cherif-Antar et al. 2016; Soares et al. 2011). The microorganisms, separated from the surfaces by various methods, are then isolated and counted by Department of Food Engineering, Hacettepe University, Beytepe, Ankara, Turkey cultural methods following inoculation into selective and/or non-selective media. Various methods can be used for the Department of Nanotechnology & Nanomedicine, Hacettepe University, Beytepe, Ankara, Turkey isolation of biofilm-forming microorganisms from surfaces. These methods include the use of swabs (Marques et al. Department of Chemical Engineering, Hacettepe University, Beytepe, Ankara, Turkey 2007; Valeriano et al. 2012), humidified swabs (Lortal et al. 896 Ann Microbiol (2019) 69:895–907 2009; Waines et al. 2011), gauze (Tang et al. 2011), scraping Materials and methods (Frank and Koffi 1990), sponges (Knight and Craven 2010), sonication and centrifugation (Bjerkan et al. 2009; Kajiyama Isolation and identification of microorganisms et al. 2009), surface washing, immersion in a washing from a dairy plant solution, agar sausage (Harrigan 1998), cutting (Lortal et al. 2009), and vortexing (Mustapha and Liewen Microbiological samples were taken from 13 sampling points 1989). from a dairy plant in Ankara, Turkey, in order to isolate Identification of the microorganisms is generally carried surface-associated microorganisms. The sampling points out by morphological, physiological, and biochemical tests. were: (1) raw milk tank, (2) pasteurized milk tank, (3) starter Biochemical tests usually include API test kits (BioMérieux, tank, (4) yogurt-filling unit (350 g), (5) yogurt filling unit France) (Bağcı 2012; Brolazo et al. 2011; Palmer et al. 2010). (1500 g), (6) white cheese tank, (7) white cheese-pressing Traditional microbiological techniques require a long time and cloth, (8) kashar maturing bench, (9) old kashar maturing a lot of chemicals, media, and labor. However, these tech- bench, wood, (10) butter tank, (11) ice cream filling unit, niques may also be insufficient for identifying species when (12) ice cream air pressing pipe, and (13) condensed milk used alone. In addition to these tests, microorganisms can be pipe. Sampling was generally repeated twice, before and after identified by molecular microbiological techniques such as the cleaning/disinfection step. Samples were assigned a two- determination of DNA base composition (using PCR tech- digit code, the first digit indicating the sampling point, and the niques), DNA hybridization tests, FISH (fluorescence in situ second digit indicating whether sanitation has been applied or hybridization), and 16S rRNA gene sequencing (Palmer et al. not, with 1 and 2 representing that the sample was taken either 2010; Waines et al. 2011). before or after the sanitation step, respectively. The surface properties of microorganisms are important Microbiological sampling was carried out by rubbing a factors in the mechanisms of adhesion. The term macroscopic moistened swab (with 0.1% buffered peptone water) strongly hydrophobicity refers to the wettability of a surface in an air in different directions on the sampling surface. The swabs environment (Ukuku and Fett 2002). Microbial hydrophobic- were then immersed in tubes containing 2 mL of Tryptic ity is an important factor that affects adhesion to a surface, i.e., Soy Broth (TSB, Sigma-Aldrich), and the tubes were vortexed biofilm formation. Microbial hydrophobicity can be deter- for 2 min to allow the passage of microorganisms into the mined by methods such as microbial adhesion to hydrocarbon broth (Marques et al. 2007; Valeriano et al. 2012; Waines test or through hydrophobic interaction chromatography et al. 2011). (Rijnaarts et al. 1995). The agar media and incubation temperatures used for the Studies have shown that both adherence-cohesion interac- isolation of microorganisms are shown in Table 1. tions on a surface and the ability of the microorganisms to Microbiological cultivation was carried out using the produce extracellular polymeric substances (EPS) are impor- spread plate technique as two replicates (Harrigan 1998; tant for adhesion (Chen and Stewart 2002;Drenkard 2003). It Temiz 2010). Inoculated Petri dishes were incubated at the has also been shown that EPS production is a precondition for optimum growth temperature of the target microorganisms supporting the formation of biofilms on surfaces and enhanc- (Table 1). The incubation times were 24–48 h for the bacteria ing adhesion. Therefore, it is of great importance to under- and 24–96 h for the yeasts. After incubation, the colonies stand the ability of surface-adhering microorganisms to pro- developed on the agar media were examined to assess their duce EPS and to understand the content of EPS they produce. morphological characteristics, and colonies showing different The aim of this study was first to determine the surfaces morphological characteristics were selected and their pure cul- having a potential risk of biofilm formation in dairy plants. tures were obtained. In order to obtain pure cultures, the indi- For this purpose, microorganisms were isolated from a dairy vidual colonies firstly re-streaked onto the same selective me- plant in Ankara. Isolation was applied from the surfaces with a dia which they were isolated from, and then the colonies high probability of biofilm formation by using general and which were grown on the selective media were re-streaked selective media. The selected isolates were identified by mor- onto the nutrient agar (Merck) plates. Isolated pure cultures phological, physiological, and biochemical tests and 16S were maintained as stock cultures at − 80 °C in a brain rRNA gene sequencing. The selected isolates were evaluated heart infusion (BHI, Merck) broth medium containing based on their ability to produce EPS and their morphological 20% glycerol (v/v) for further analysis. Intermediate structure. The surface properties of the microorganisms were stock cultures were prepared using nutrient agar slant assessed using the microbial adhesion to hydrocarbons from the stock cultures, and they were stored in a re- (MATH) test, the static water contact angle test, the salt ag- frigerator at 0–5 °C with regenerating every 3 months. gregation test, and the surface zeta potential test. EPS were From these intermediate stock cultures, 24-h cultures isolated from microorganisms and their total sugar, uronic were obtained in a nutrient broth (Merck) medium and acid, and neutral sugar contents were determined. they were used for further analysis. Ann Microbiol (2019) 69:895–907 897 Table 1 The agar media and The agar media Target Incubation incubation temperatures used for microorganisms temperature (°C) the isolation of the target microorganisms Violet red bile dextrose agar (VRBDA, Merck) Enterobacteriaceae members 37 ± 1 Fluorocult violet red bile agar (Merck) E. coli 37 ± 1 Baird parker agar (BPA, Oxoid) Staphylococcus spp. 37 ± 1 Pseudomonas agar base (PA, Sigma-Aldrich) with CFC Pseudomonas spp. 37 ± 1 (cetrimide, fucidin, cephalosporin) supplement Lactobacillus agar acc. to De Man, Rogosa and Sharpe Lactobacillus spp. 30 ± 1 (MRS agar, Sigma-Aldrich) M17 agar (Oxoid) Lactococcus spp. 37 ± 1 Chromogenic Listeria agar (OCLA, Oxoid) Listeria spp. 37 ± 1 Dextrose casein-peptone agar (DCPA, Merck) Bacillus spp. 37 ± 1 Brilliant green phenol red lactose sucrose agar Salmonella spp. 37 ± 1 (BPLS Agar, Merck) Yeast extract agar (YEA, Sigma-Aldrich) Yeasts 30 ± 1 The microscopic morphology of each pure culture was de- Madison, WI, USA). Sequence results were evaluated using termined and an API test kit (bioMérieux, France) was used to the NCBI BLAST program. identify them at the species level. The API test kits used were as follows: API 20 E for Enterobacteriaceae members; API Surface properties of microorganisms 20 NE for Pseudomonas spp.; API Staph for Staphylococcus spp.; API Listeria for Listeria spp.; API 50CHB for Bacillus Microbial adhesion to hydrocarbons, static water contact spp.; API 50CHL for Lactobacillus spp.; API Strep for angle, salt aggregation, and surface zeta potential test Lactococcus spp.; and API 20C AUX for yeasts. measurements were performed in triplicate as described API test kits do not always give consistent results for the below. identification of lactic acid bacteria (Brolazo et al. 2011; Martín et al. 2010). To ensure the discrimination of Microbial adhesion to hydrocarbons test lactic acid bacteria, some basic morphological, physio- logical, and biochemical tests (Gram staining, catalase The cell surface hydrophobicity of the identified microorgan- activity, gas production from growth in glucose, growth isms was determined using the microbial adhesion to hydro- at 10 °C and 45 °C, growth in 2%, 4%, and 6% salt- carbons test and reported as % H. The absorbance values of containing media, growth at pH 9.6, arginine hydrolysis, 24-h cell cultures before and after the application of n-decane and an hemolysis test) were also used to assess (BDH Chemicals, UK) were measured at 400 nm using a suspected isolates of lactic acid bacteria from the MRS spectrophotometer (Thermo Scientific, iCE 3000 Series agar and M17 agar media. Atomic Absorption Spectrometers, USA) (Rosenberg To identify pure cultures at the species level, the isolates et al. 1980). In this method, the absorbance value be- were also subjected to 16S rRNA gene sequencing using uni- fore the n-decane application (A ) was firstly measured versal primers (Sanger et al. 1977). DNA extraction was per- 0 by the spectrophotometer. Then 1 mL of n-decane was formed using Qiagen DNeasy Blood & Tissue Kit (Qiagen added onto 3 mL culture suspension. The suspension Inc., Valencia, CA). The 16S rRNA genes were amplified wasthenvortexedfor 2minandallowedtostandfor using the primer pairs of 27F (5′-AGA GTT TGA TCC 15 min to remove the hydrocarbon. The absorbance val- TGG CTC AG) and 907R (5′-CCC CGT CAA TTC ATT ue after the n-decane application (A) was measured by TGA GTT T). The PCR mix (50 μL) was prepared from the spectrophotometer from the underlying phase of the 1 μL dNTP, 5 μL 10× buffer, 0.3 μL 27F primer, 0.3 μL two-phase mixture. Surface hydrophobicity (% H) was 907R primer, 0.3 μL Taq polymerase (Boehringer GmbH, determined using the following formula. Mannheim, Germany), and 2 μLMgCl . Five hundred nano- grams of DNA extract was amplified with the PCR mix. %H ¼½ ðÞ A –A =A 100 Polymerase chain reaction amplification was performed with 0 0 the following thermal conditions: 94 °C for a 2-min step, 30 cycles of 94 °C for 30 s, 58 °C for 30 s, 72 °C for 30 s, and finished by a 72 °C for a 5-min step. PCR purification was A The absorbance value before the n-decane application applied with Promega PCR Purification kit (Promega, A The absorbance value after the n-decane application 898 Ann Microbiol (2019) 69:895–907 Static water contact angle test Determination of uronic acid The static water contact angle values of the identified micro- The uronic acid content of the isolated EPS was determined organisms were determined using the sessile drop method spectrophotometrically following conversion to galactonic ac- described by Absolom et al. (1983). Three replicates were id (Blumenkrantz and Asboe-Hansen 1973). studied for each measurement using a goniometer (Krüss DSA 100, Germany) at room temperature. Determination of neutral sugar The neutral sugars predominant in the EPS derived from each Salt aggregation test microorganism were identified using GC-MS. EPS (10– 100 μg) were first treated with 0.5 N NH OH solution Eighty microliters 24-h culture was transferred to 80 μLam- (100 μL) and incubated at room temperature for 10–15 min monium sulphate solution at different concentrations in a closed tube. Next, 1 mg of NaBH was added and the (between 0.01 and 4 M) in each well of a cavity slide. solution was kept closed for 10 min at 100 °C. At this stage, Crystal violet was added to make the agglutinates visi- aldoses are reduced to alditols. The tube contents were dried at ble. The salt aggregation test (SAT) value was obtained 55 °C. Excess NaBH was cleaved by the addition of 100 μL by observing the lowest concentration of ammonium of 2 M trifluoroacetic acid. Then, 100 μLof methanol was sulfate that produces visible agglutinates (Styriak et al. added and the solution was dried at 55 °C to remove the 1999). cleavage products (repeated two times). The residue was dis- solved with 0.5 M HCl (200 μL) in methanol, and the solution was kept closed at 100 °C for 15 min and dried at 55 °C. Surface zeta potential test During this step, the alditols are derivatized to methyl ester alditol forms. These methyl ester alditols were acetylated by Before measurements, the 24-h cultures (viable cell number: adding a mixture of pyridine-acetonitrile (200 μL; 1:1, v/v) 1.5 × 10 CFU/mL) of test microorganisms were prepared. and incubated at 100 °C for 30 min in a closed tube. The Measurements were then made using a Zetasizer (3000HSA, percentage distribution of neutral sugars in the EPS solution Malvern Instruments, UK). isolate was quantitatively determined using GC-MS with a TRACE DSQII (Thermo Fisher Scientific, Waltham, MA, USA) (Sassaki et al. 2008). Isolation of exopolysaccharides The conditions used for the GC-MS analysis were as fol- lows: injector, split mode; injection volume 2 μL; detector MS The microorganism was inoculated into 10 mL of sterile DSQII; column: 7HG-G006–11 Zebron ZB-1701 capillary skimmed milk, and incubated at 37 °C for 24 h. One milliliter GC column (30 m × 0.25 mm × 0.25 μm, Phenomenex); car- of 4% trichloroacetic acid (v/v) was then added to each culture rier gas: helium (1 mL/min); mass range 35–500; temperature to precipitate proteins and cells, and the mixture was incubat- program: 60 °C for 5 min, 60 °C–270 °C at 10 °C/min, 270 °C ed in a shaking water bath at 37 °C for 2 h. The sus- for 15 min; ion source temperature: 230 °C; transfer line tem- pension was centrifuged for 35 min at 10,000×g at perature: 270 °C. 4 °C, and the supernatant was separated and filtered through a 0.45-μm membrane filter (Millipore, USA). Following this, 96% cold ethyl alcohol (v/v) was added Results to the supernatant at ratios of 1:1, 1:2, and 1:3 followed by centrifugation at 5000×g for 15min at 4°Cafter Isolation and identification of microorganisms each treatment. The resulting EPS were dissolved in from the dairy industry 1 mL of water and filtered through a 0.45-μmmem- brane filter. Finally, the EPS were obtained in dry form Totally, 495 isolates were obtained using the different agar by lyophilization using a freeze dryer (ALPHA 1–4 media. Among these, 36 were isolated from VRBDA, 38 from LDplus, Christ, Germany) (Yang 2000). FVRBA, 34 from BPA, 19 from PA, 55 from MRS agar, 78 from M17 agar, 17 from OCLA, 66 from DCPA, 20 from Determination of total sugar BPLS agar, and 132 from YEA media. Of the 495 colonies isolated, there were 163 typical and 332 atypical colonies. The total sugar was determined spectrophotometrically Totally, 170 isolates were obtained after the sanitation steps using the phenol sulfuric acid method described by in the dairy plant. These microorganisms were isolated after DuBois et al. (1956). the cleaning/disinfection processes of the tanks of pasteurized Ann Microbiol (2019) 69:895–907 899 milk, white cheese and butter, the filling units of yogurt and species level compared with the identification of other bacteria ice cream, and the pipes of ice cream air pressing and con- and yeasts. densed milk. Eighty-six out of 170 isolates produced mucous colonies. Surface properties of microorganisms The isolated microorganisms were grouped according to diversity in their macroscopic (colony shape and structure, In these experiments, S. aureus ATCC 25923 and E. coli typical or atypical colony formation, etc.) and microscopic ATCC 25922 strains were used as standard control microor- morphologies, Gram-staining reactions (for bacteria), physio- ganisms, in addition to the 10 test microorganism isolates. logical and biochemical test results, behavior in the dairy in- dustry (saprophyte or fecal contamination indicator), their Microbial adhesion to hydrocarbons test pathogenicity, and toxicity. Among these, 42 isolates were selected for identification at the species level using API test The MATH test surface hydrophobicity values of the 10 se- kits and 16S sequence analysis. These 42 isolates, identified lected isolates and the controls are shown in Table 3. Among by API and 16S rRNA gene sequencing, were re-grouped the surface tests, the MATH test exhibited the lowest standard according to diversity in their macroscopic (colony shape deviations, and the most consistent results between the and structure, typical or atypical colony formation, etc.) and replicates. microscopic morphologies, Gram-staining reaction (for bacte- The MATH test is one of the criteria used to evaluate the ria), the results of physiological and biochemical tests, API surface adhesion potential of microorganisms. A value greater tests and 16S rRNA gene sequencing, pathogenicity and tox- than 70% indicates that a test microorganism is hydrophobic, icity potential, spoilage-forming potential in milk and values from 30 to 70% indicate it is weakly hydrophobic, and dairy products, and whether they were microorganisms values less than 30% indicate it is hydrophilic (Abasolo- indicative of fecal contamination. Following this, 10 Pacheco et al. 2015;Kwaszewska etal. 2006). It is thought isolates were selected from 42 isolates considering the that hydrophilic MATH values of microorganisms increase isolate re-groups mentioned above and studied further. surface adhesion. Besides the microorganisms, surfaces also The identity of these isolates is shown in Table 2 along have hydrophilic or hydrophobic characteristics. In the food with their isolation surface, isolate codes, isolation me- industry, stainless steel surfaces are frequently used, and the dia, and their identity obtained through 16S rRNA gene hydrophilic property of these stainless steel surfaces is an im- sequencing at the species level. Some of the microor- portant factor in biofilm formation (Frank 2001). ganisms mentioned in Table 2 were isolated from selec- In general, the surface hydrophobicity values of the test tive media that are used for the selection of other mi- microorganisms were positive. However, some test microor- croorganisms instead of from their own selective media. ganisms (K. variicola, E. coli, P. mirabilis,and E. coli ATCC API test kits usually produce accurate results when defin- 25922) had negative values. In general, the literature reports ing many bacterial groups. In this study, the results obtained that the surface hydrophobicity values of microorganisms are with the API test kits were found to be consistent with the positive. It has however also been reported in the literature that results obtained with 16S rRNA gene sequencing, but there some microorganism strains have negative values. For exam- were differences at the species level. For Staphylococcus spe- ple, the surface hydrophobicity values of E. coli strains by cies, the identification results obtained using 16S rRNA gene usingdodecanehavebeenreportedasbeing − 2.0% and − sequencing were more consistent with the API results at the 6.0% by Saini (2010). This is because some hydrocarbons can Table 2 Microorganisms selected Isolation surface Isolate code Identity for further study Condensed milk pipe YEA 13.2.1 Enterococcus faecalis Yogurt filling unit, 1500 g BPA 5.2.2 Staphylococcus epidermidis Raw milk tank M17 1.1.1 Lactococcus garvieae Condensed milk pipe M17 13.1.2 Lactococcus garvieae Yogurt filling unit, 1500 g YEA 5.2.6 Bacillus toyonensis Raw milk tank FVRBA 1.1.5 Pseudomonas aeruginosa White cheese pressing cloth VRBDA 7.1.1 Escherichia coli White cheese pressing cloth FVRBA 7.1.2 Klebsiella variicola Yogurt filling unit, 350 g MRS 4.2.1 Candida parapsilosis Raw milk tank VRBDA 1.1.1 Proteus mirabilis 900 Ann Microbiol (2019) 69:895–907 Table 3 Surface test values of the isolates Isolate Code Microorganism MATH Test surface Static water SAT (Molar)* Surface Zeta hydrophobicity (%)* contact angle (°)* Potential (mV)* FVRBA 1.1.5. Pseudomonas aeruginosa 10.6 ± 0.5** 26.0 ± 5.1 2.5 −5.9 ± 4.1** M17 1.1.1. Lactococcus garvieae 25.1 ± 0.7 0.0 ± 0.0 1.5 −16.9 ± 3.8 M17 13.1.2. Lactococcus garvieae 29.2 ± 0.7 12.0 ± 3.3 <0.01 −15.6 ± 4.6 YEA 5.2.6. Bacillus toyonensis 30.4 ± 0.2 33.0 ± 4.5** 3.0 ** −8.8 ± 0.2 YEA 13.2.1. Enterococcus faecalis 35.1 ± 1.1 24.0 ± 1.9 <0.01 −11.5 ± 3.0 MRS 4.2.1. Candida parapsilosis 45.7 ± 0.1 0.0 ± 0.0 2.0 −7.9 ± 0.7 BPA 5.2.2. Staphylococcus epidermidis 74.4 ± 0.6 25.0 ± 7.2 <0.01 −13.1 ± 4.2 ATCC 25923 Staphylococcus aureus 94.2 ± 0.2 6. 0 ± 4.5 <0.01 −13.7 ± 6.0 FVRBA 7.1.2. Klebsiella variicola − 10.6 ± 0.0 22.0 ± 2.0 0.4 −11.4 ± 4.8 ATCC 25922 Escherichia coli − 8.9 ± 0.1 21.0 ± 3.0 <0.01 −18.4 ± 1.5 VRBDA 7.1.1. Escherichia coli − 7.5 ± 0.4 18.0 ± 7.4 2.5 −7.4 ± 2.3 VRBDA 1.1.1. Proteus mirabilis − 5.9 ± 0.3 0.0 ± 0.0 2.5 −11.0 ± 4.4 *Measurements were performed in triplicate, and results are presented as mean ± standard deviation **The best result for each test in terms of adhesion capability diffuse in water, resulting in a higher final absorbance value values of S. epidermidis strains were reported to be 4.0, 7.0, (A) than the initial absorbance value (A ). However, in such 8.0, and 55.0% (Hanlon et al. 1999). cases, evaluation can be made using other different hydrocar- In this study, the control E. coli ATCC 25922 strain and the bons like octane (Saini 2010). test E. coli strain gave similar results, and similar results were When the negative values were ignored, P. aeruginosa and observed between the control S. aureus ATCC 25923 strain both of the L. garvieae isolates were the most hydrophilic and the test S. epidermidis strains. microorganisms isolated. These isolates were followed by B. toyonensis, which had a relatively lower hydrophilic charac- Static water contact angle teristic. The most hydrophobic isolates were C. parapsilosis and S. epidermidis. The control S. aureus The static water contact angles of the 10 selected isolates and ATCC 25923 strain was the most hydrophobic microor- the controls are shown in Table 3. ganism, giving a 94.2 ± 0.2% value, whereas the control The surface adhesion potential of microorganisms can be E. coli ATCC 25922 strain gave the most negative sur- evaluated by measuring the static water contact angle. In the face hydrophobicity value. literature, it is reported that there is a positive correlation be- Surface property values may vary strain to strain. On the tween the static water contact angle and the ability of micro- other hand, the MATH values obtained for the tested micro- organisms to adhere to the surface (Boonaert et al. 2001;Li organisms are generally consistent with the results reported in and Logan 2004). the literature for the same species (Hamadi and Latrache 2008; When the static water contact angle values of the isolates Li and McLandsborough 1999; Minagi et al. 1986). Since were examined, B. toyonensis and P. aeruginosa exhibited the information about the MATH values for L. garvieae and B. highest, whereas C. parapsilosis and P. mirabilis exhibited the toyonensis is not available in the literature, the MATH values lowest values (Table 3). It can be said that B. toyonensis and P. for L. garvieae and B. toyonensis were compared with those of aeruginosa have the highest adhesion capability based on L. lactis and B. subtilis, respectively. In the literature, the static water contact angle results. MATH value for L. lactis wasreportedas34.0% (Marín The surface properties may vary on the strain basis. For et al. 1997), whereas the MATH value for B. subtilis was example, the static water contact angle values of P. aeruginosa reported as 28.0% (Abasolo-Pacheco et al. 2015). strains have been reported to be 36° (Pasmore et al. 2001), Surface hydrophobicity values of the microorganisms vary between 21 and 85°, generally between 65 and 85° greatly depending on the strain. For example, the surface hy- (Triandafillu et al. 2003). Moreover, the static water contact drophobicity values of the P. aeruginosa strains were reported angle values in present study are generally consistent with the to lie within the range 12.0–84.0% (Vanhaecke et al. 1990), literature for the same species (Feng et al. 2009;Hamadi and whereas the surface hydrophobicity values of S. epidermidis Latrache 2008; van Merode et al. 2008). Because of the lack strains were reported to range between 22.0 and 81.0% (Jones of information in the literature about the static water contact et al. 1996). In another report, the surface hydrophobicity angle values for B. toyonensis, the static water contact angle Ann Microbiol (2019) 69:895–907 901 values for B. toyonensis were compared with those for B. microorganism increases, which causes its hydrophobicity to subtilis or B. cereus. The static water contact angle values increase. Because of this increase in hydrophobicity, the abil- for B. subtilis have been reported as being between 33 and ity of the microorganism to adhere to surfaces decreases. The 59°, generally 40°, for the vegetative forms, and between 20 surface zeta potential value is determined using the absolute and 45°, generally 30 , for the spore forms (Ahimou et al. value of the data. Microorganisms with small absolute surface 2001). The static water contact angle value of B. cereus has zeta potential values have a high surface binding ability. In been reported as being 25° (Bernardes et al. 2010). other words, the absolute surface zeta potential value and the ability of microorganisms to adhere to surfaces are inversely Salt aggregation test proportional (Li and Logan 2004). When the absolute surface zeta potential values of the iso- The SAT values of the 10 selected isolates and the controls are lates were examined, P. aeruginosa and E. coli exhibited the shown in Table 3. lowest, whereas L. garvieae (M17 1.1.1. and M17 13.1.2.) and The salt aggregation test gives information about the sur- S. epidermidis exhibited the highest values (Table 3). It can be face adhesion of microorganisms. Cultures with SAT values of said that P. aeruginosa and E. coli have the highest adhesion 0.01 to 0.2 M are considered highly hydrophobic, while those capability, whereas L. garvieae (M17 1.1.1. and M17 13.1.2.) of 0.2 to 1.5 M are considered hydrophobic, and cultures with and S. epidermidis have the lowest adhesion based on absolute SAT values greater than 1.5 M are considered hydrophilic surface zeta potential results. (Styriak et al. 1999). Microorganisms with hydrophilic SAT Even a different strain of a species may have different sur- values demonstrate a greater ability to adhere surfaces. Hence, face properties. For example, the surface zeta potential values B. toyonensis, P. aeruginosa, E. coli, P. mirabilis,and C. of P. aeruginosa strains have been reported to be − 9.0 and − parapsilosis were found to be hydrophilic, L. garvieae (M17 16.0 mV (Gómez-Suárez et al. 2002). The surface zeta poten- 1.1.1.) and K. variicola were hydrophobic, and E. faecalis, S. tial values of the S. epidermidis strains have been reported as epidermidis,and L. garvieae (M17 13.1.2.) were highly hy- being between − 6.0 and − 10.0 mV (Gallardo-Moreno et al. drophobic. The control strains E. coli ATCC 25922 and S. 2009). On the other hand, surface zeta potential results were aureus ATCC 25923 were also highly hydrophobic obtained in accordance with the literature (Li and (Table 3). It can be said that B. toyonensis, P. aeruginosa, E. McLandsborough 1999;Wanget al. 2012). The B. toyonensis coli, and P. mirabilis have the highest adhesion capability, surface zeta potential values were compared with those of B. whereas E. faecalis, S. epidermidis, and L. garvieae (M17 subtilis or B. licheniformis because there is not any study 1.1.1.) have the lowest adhesion based on salt aggregation test about this. The surface zeta potential values of B. subtilis have results. been reported as being between − 15.0 and − 50.0 mV The surface properties may vary even in different strains of (Ahimou et al. 2001). The B. licheniformis surface zeta poten- a species. For example, the SAT values of P. aeruginosa tial values have been reported as being between − 16.0 and − strains have been reported to be within the range 0.0–4.0 M 43.0 mV (Li et al. 2009). (Vanhaecke et al. 1990). The SAT values of S. aureus strains have been reported to be < 0.1 M (Ljungh et al. 1985)or Exopolysaccharide composition between 0.025–2.0 M (Ljungh and Wadström 1995). Otherwise, considering the same species, SAT results are Total sugar and uronic acid mostly consistent with the literature (Arana et al. 1999; Marín et al. 1997). In as much as there is no information about The total sugar and uronic acid contents of the EPS produced the SAT values for B. toyonensis in the literature, they were by the 10 selected isolates are shown in Table 4. compared with those for B. thuringensis, B. licheniformis,or In literature, the results for the total sugar of the isolates are B. cereus. These latter species have been reported as having generally consistent with those for total uronic acid content SAT values of 2.0 M, 1.8 M, and 0.2 M, respectively (Strathmann et al. 2002). The results of the present study were (Obuekwe et al. 2009). also consistent in terms of total sugar and uronic acid content. P. aeruginosa showed the highest sugar- and uronic acid– Surface zeta potential test producing abilities followed by S. epidermidis.Boththe L. garvieae isolates showed the lowest sugar-producing ability, The surface zeta potential values of the 10 selected isolates followed by E. coli.However,these two L. garvieae isolates and the controls are shown in Table 3. were followed by P. mirabilis in terms of the lowest uronic The surface zeta potential is used to assess the potential of acid content. B. toyonensis showed relatively lower sugar- and microorganisms to adhere various surfaces. The value of the uronic acid–producing abilities compared with P. aeruginosa. surface zeta potential depends on ionic strength. As the ionic The ability to produce EPS by a microorganism, as well as strength increases, the surface zeta potential value for a the EPS content, is thought to be major contributors to 902 Ann Microbiol (2019) 69:895–907 Table 4 Total sugar and uronic Isolate code Microorganism Total sugar Uronic acid acid contents 9 9 (μg/10 cells) (μg/10 cells) FVRBA 1.1.5. Pseudomonas aeruginosa 1900 108 BPA 5.2.2. Staphylococcus epidermidis 1560 89 VRBDA 1.1.1. Proteus mirabilis 1368 62 FVRBA 7.1.2. Klebsiella variicola 1357 65 MRS 4.2.1. Candida parapsilosis 1333 69 YEA 5.2.6. Bacillus toyonensis 1227 63 YEA 13.2.1. Enterococcus faecalis 1050 72 VRBDA 7.1.1. Escherichia coli 1012 66 M17 13.1.2. Lactococcus garvieae 837 58 M17 1.1.1. Lactococcus garvieae 790 52 adhesion and biofilm formation on surfaces. Uronic acid is the ribose by C. parapsilosis, and sorbitol and mannose by E. most abundant acidic sugar found in the EPS. Therefore, coli (Table 5). assessing the EPS production ability of the test microorgan- The following sugars have been demonstrated to be present isms, and measuring the total sugar and uronic acid, may be in the EPS from different microorganisms: ribose, arabinose, most predictive of the ability of a microorganism to adhere mannose, glucose, and galactose in the EPS from the Bacillus surface. As mentioned earlier, P. aeruginosa and B. toyonensis spp. (Fox 1999); glucose, xylose, and rhamnose in the EPS exhibited the best results based on the surface tests. When from the P. aeruginosa (Yokota et al. 1987); glucose, galac- these two bacteria were assessed in terms of total sugar and tose, and rhamnose in the EPS from the Enterococcus spp. uronic acid in their EPS, P. aeruginosa was found to have a (Mozzi et al. 2006); fucose and galactose in the EPS from much better results than B. toyonensis. the L. lactis subsp.lactis (Suzuki et al. 2013); glucose, man- In one study, the total carbohydrate content of P. nose, galactose, and arabinose in the EPS from the C. aeruginosa was found to be 705–749 μg/10 cells in the bio- albicans (Kiran et al. 2015); and mannose, galactose, film and 535–512 μg/10 cells in the EPS. Moreover, the glucose, galactonic acid, arabinose, fucose, rhamnose, uronic acid content was found to be 408–450 μg/10 cells in and xylose in the EPS from the S. epidermidis and E. the biofilm and 354–381 μg/10 cells in the EPS (Strathmann coli (Bales et al. 2013). et al. 2002). In another study, the total carbohydrate content in EPS are microbial substances that have important contribu- P. aeruginosa was found to be 1006 μg/10 cells in the biofilm tions in the formation of biofilm. EPS are critical to the mat- and 767 μg/10 cells in the EPS. In this same study, the uronic uration of the biofilm structure as well as the initial binding acid content was found to be 474 μg/10 cells in the biofilm stage of microorganisms (Marshall 1992), (Sutherland 1982). and 403 μg/10 cells in the EPS (Wingender et al. 2001). The EPS protect the bacteria from dehydration by holding water and are drying very slowly (Ophir and Gutnick 1994), Neutral sugar content (Roberson and Firestone 1992). EPS are also important for the survival of microorganisms in adverse environmental condi- The percentage distribution of neutral sugars extracted from tions (Rinker and Kelly 1996). Moreover, the EPS are effec- each isolate is shown in Table 5. tive in keeping the nutrients for the biofilm structure to mature The neutral sugar content of the EPS may be an important and protecting the cells against antimicrobial agents. contributing factor for adhesion of microorganisms (Yang In order to eliminate microorganisms in the biofilm struc- 2000). As expected, there were large variations in the neutral ture, the biocides must penetrate to the EPS structure and sugar content in EPS produced by the different isolates reach the microorganism cells which are in the inner layers (Table 5). (Meyer 2003). Since the EPS composition differs according to Glucose and mannitol were the two most abundant two the biofilm type, different methods are used for each biofilm neutral sugars produced by P. aeruginosa, with mannose and structure. For example, oxidation agents such as peracetic acid glucose being two most abundant two neutral sugars produced and chlorine are preferred for the elimination of biofilm layers by K. varriicola, sorbitol and mannose by P. mirabilis,glu- formed by Pseudomonas and Listeria on stainless steel sur- cose and sorbitol by L. garvieae (M17 13.1.2.), glucose and faces (Jang et al. 2006). Active chlorine is preferred due to its mannose by B. toyonensis, sorbitol and glucose by S. ability to remove microorganisms in the biofilm structure as epidermidis, mannose and sorbitol by L. garvieae (M17 well as to remove EPS on the surface (Meyer 2003). Ozone is 1.1.1.), mannose and sorbitol by E. faecalis,glucose and a strong oxidizing agent and has been successfully applied to Ann Microbiol (2019) 69:895–907 903 Table 5 Percentage distribution of neutral sugars extracted from each isolate Analytical type % distribution of neutral sugars Pseudomonas Klebsiella Proteus Lactococcus Bacillus Staphylococcus Lactococcus Enterococcus Candida Escherichia aeruginosa variicola mirabilis garvieae toyonensis epidermidis garvieae faecalis parapsilosis coli (M17 13.1.2.) (M17 1.1.1.) Monosaccharides D-Glucose 30.25 17.37 24.87 27.62 28.04 24.26 11.37 11.65 37.82 14.56 α-D-Talose 8.42 4.06 0.02 0.10 0.21 0.16 5.79 2.04 5.12 1.55 α-D-Galactose 0.79 2.83 0.78 1.38 1.32 2.14 3.51 1.75 8.88 – β-D-Mannose 5.31 4.69 0.30 0.26 1.40 0.75 6.80 2.79 4.50 1.43 α-D-Mannose 9.10 29.34 15.16 18.31 22.94 15.85 16.91 21.85 4.16 18.57 α-D-Altrose – 1.34 –– – – – – 1.13 – D-Fructose – 0.02 0.01 0.02 –– 0.03 –– – α-D-Ribose –– 0.38 – 0.67 – 2.55 1.61 13.12 2.12 Disaccharides Maltose – 0.36 – 0.11 –– 0.29 0.30 – 1.04 Kojibiose –– – – – – 0.07 –– 0.21 Aldopentoses Xylose 7.77 – 0.02 –– – 1.27 –– 1.06 D-Arabinose 1.30 – 0.39 –– – – – 2.07 0.39 Sugar alcohols D-Glucitol 3.27 0.58 0.06 0.02 0.09 – 0.53 0.45 1.87 2.29 Galactitol 3.99 12.26 13.29 13.07 15.75 14.12 11.89 13.76 8.57 9.20 D-Mannitol 22.10 3.56 – 0.05 3.21 0.37 14.95 10.47 11.44 11.15 Sorbitol 7.70 17.28 30.91 25.96 20.23 28.24 15.56 20.59 – 22.56 Iditol – 3.63 13.82 13.10 6.14 14.12 8.17 12.17 – 13.52 D-Xylitol – 2.70 –– – – 0.39 0.58 1.32 0.54 B–^ means not detected 904 Ann Microbiol (2019) 69:895–907 remove biofilms from oligotrophic water systems (Barnes and air pressing pipe, butter tank, and condensed milk pipe. All Caskey 2002). these units came into direct contact with the final dairy prod- Bacteriocins are also used to minimize the biofilm forma- uct. This is important in terms of food hygiene and food qual- tion of foodborne pathogenic microorganisms. It was stated ity, so further precautions should be taken in this particular that the use of plantaricin 423, pediocin PD-1, and nisin was dairy plant. effective against the biofilm structure formed by Oenococcus API test kits and 16S rRNA gene sequencing results were oeni (Nel et al. 2002). Moreover, EPS also increase the resis- consistent at the genus level, but there were some differences tance of microorganisms to cleaning agents. It was reported at the species level. The species level identification was most that the catalase enzyme in biofilm structure of P. aeruginiosa consistent for Staphylococcus but varied significantly for lac- was effective in reducing the efficacy of hydrogen peroxide- tic acid bacteria and yeasts. containing disinfectants (Stewart et al. 2000). Within the scope of this study, the surface properties of 10 In the present study, the EPS-producing ability of surface selected isolates were determined to assess their ability for sur- adhesive microorganisms in a dairy plant and the content of face adhesion. Among the surface tests, the MATH test exhibited EPS they produce were determined. The data about EPS con- the lowest standard deviations, and the most consistent results tent of the isolates shed some light on the determination of the between the replicates. It can be said that, MATH test is the most chemicals which should be preferred for effective cleaning/ useful test in determining the surface properties of microorgan- disinfection in a dairy plant. isms with respect to surface adhesion. The hydrophilic character of microorganisms provides higher surface adhesion potential. P. aeruginosa, a Gram-negative isolate, and B. toyonensis,a Gram- Discussion positive isolate, exhibited the best results in terms of surface test. The ability of the test bacteria to produce exopolysaccharides, In this study, several microorganisms were isolated from dif- which are a major contributor to adhesion, is thought to be related ferent sampling points in a dairy plant. The microorganisms more to biofilm formation on the surface than on the cell’s ability were isolated after cleaning/disinfection to a similar degree as to adhere to the surface. In addition, the total sugar and uronic before cleaning/disinfection of the sampling points in the acid content have great importance during the assessment of dairy plant. The microorganism isolates included microorgan- surface adhesion. When the exopolysaccharides from these two isms that may be pathogenic or are opportunistic pathogens, or bacteria were assessed in terms of total sugar and uronic acid, P. could potentially affect other microorganisms and cause a de- aeruginosa was indicated to have better results than B. terioration of the milk and dairy products. Some sampling toyonensis. Moreover, neutral sugar was determined in their points drew attention as being processing points that may alditol acetate forms by using gas chromatography–mass spec- trometry. Awide variety of neutral sugar content was determined cause post-production contamination. Stainless steel is the most preferred material on the surface foreachofthe isolates. P. aeruginosa had richer neutral sugar of the equipment and materials used in the food industry, and content in its exopolysaccharide than that of B. toyonensis.Asa the hydrophilic property of these surfaces is an important fac- result, it is believed that determination of the EPS content would tor in biofilm formation (Frank 2001). In literature, it was contribute to establishing of the effective cleaning/disinfection shown that the critical surface tension value promotes the procedure for dairy plants. attachment of microorganisms to various surfaces In the next step of the study, the biofilm formation will be (Boulange-Petermann et al. 1993), (Bryers 1987). As the free investigated with these two test bacteria (P. aeruginosa and B. surface energy and the wettability of the surface increase, the toyonensis) by using stainless steel plates in batch and flow binding of the bacterial cells to the surface approaches the growth media. maximum level. The surfaces with high free surface energy Funding information This work was supported by the Hacettepe such as stainless steel and glass are more hydrophilic. These University Scientific Research Projects Coordination Unit (Project surfaces cause higher bacterial binding and thus cause more Codes: 014 D01 602 003 and FDK-2016-13096). biofilm formation compared with hydrophobic surfaces such as Teflon, nylon, and rubber (Blackman and Frank 1996), Compliance with ethical standards (Hyde et al. 1997), (Mafu et al. 1990), (Sinde and Carballo 2000). In a study by Smoot and Pierson (Smoot and Pierson Conflict of interest The authors declare that they have no conflict of 1998), it was noted that Listeria monocytogenes attaches interest. faster but stronger to stainless steel surfaces than rubber Research involving human participants and/or animals This article surfaces. does not contain any studies with human participants or animals per- In this study, numerous microorganisms were isolated after formed by any of the authors. cleaning and disinfection of the pasteurized milk tank, yogurt filling unit, white cheese tank, ice cream filling unit, ice cream Informed consent Not applicable. Ann Microbiol (2019) 69:895–907 905 Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of References clinically relevant microorganisms. 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Annals of Microbiology – Springer Journals
Published: May 23, 2019
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