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Isolation and characterization of a lead (Pb) tolerant Pseudomonas aeruginosa strain HF5 for decolorization of reactive red-120 and other azo dyes

Isolation and characterization of a lead (Pb) tolerant Pseudomonas aeruginosa strain HF5 for... Presence of heavy metals including lead (Pb) in the textile effluents is a crucial factor affecting the growth and potential of the dye decolorizing bacterial strains. This work was planned to isolate and characterize a bacterial strain exhibiting the potential to decolorize a range of azo dyes as well as the resistance to Pb. In this study, several Pb tolerant bacteria were isolated from effluents of textile industry. These bacterial isolates were screened for their potential of decolorizing the reactive red-120 (RR120) azo dye −1 with presence of Pb (50 mg L ). The most efficient isolate was further characterized for its potential to resist Pb and decolorize different azo dyes under varying cultural and incubation conditions. Out of the total 82 tested bacterial isolates, 30 bacteria were found to have varying potentials to resist the presence of lead (Pb) and carry out decolorization of an azo dye reactive red-120 −1 (RR120) in the medium amended with Pb (50 mg L ). The most efficient selected bacterium, Pseudomonas aeruginosa strain HF5, was found to show a good potential not only to grow in the presence of considerable concentration of Pb but also to decolorize RR120 and other azo dyes in the media amended with Pb. The strain HF5 completely (> 90%) decolorized RR120 in mineral salt −1 −1 medium amended with 100 mg L of Pband20gL NaCl. This strain also considerably (> 50%) decolorized RR120 up to the −1 −1 presence of 2000 mg L of Pband50gL of NaCl but with reduced rate. The optimal decolorization of RR120 by HF5 was −1 achieved when the pH of the Pb amended (100 mg L ) mineral salt media was adjusted at 7.5 and 8.5. Interestingly, this strain also showed the tolerance to a range of metal ions with varying MIC values. The Pseudomonas aeruginosa strain HF5 harboring the unique potentials to grow and decolorize the azo dyes in the presence of Pb is envisaged as a potential bioresource for devising the remediation strategies for treatment of colored textile wastewaters loaded with Pb and other heavy metal ions. . . . . Keywords Pseudomonas aeruginosa Lead (Pb) tolerance Azo dyes decolorization Heavy metal tolerance NaCl resistance Introduction Farhan Hafeez and Huma Farheen contributed equally to this work. Electronic supplementary material The online version of this article Textile effluents are a major source of freshwater pollution which (https://doi.org/10.1007/s13213-018-1403-6) contains supplementary have been reported to have impacts on different ecological com- material, which is available to authorized users. ponents of the environment as well as the human beings (Chequer et al. 2009;Khanand Malik 2014;Guptaetal. 2015; * Sabir Hussain sabirghani@gmail.com Imran et al. 2015a). These impacts are primarily attributed to- wards the occurrence of enormous amounts of synthetic dyes and Department of Environmental Sciences, COMSATS University heavy metals in the textile effluents (Khan and Malik 2014; Islamabad, Abbottabad Campus, Tobe Camp University Road, Imran et al. 2015a). Reports have suggested that an average Abbottabad 22060, Pakistan −1 concentration of dye may exist up to 300 mg L in the effluent Department of Environmental Sciences & Engineering, Government generated from the textile industries (Tony et al. 2009)which is College University, Allama Iqbal Road, Faisalabad 38000, Pakistan −1 less frequent than the 10–250mgL value as reported by Department of Bioinformatics and Biotechnology, Government O’Neill et al. (1999). Literature has reported as high as College University, Allama Iqbal Road, Faisalabad 38000, Pakistan −1 1500 mg L of dyes in some textile effluents (Pierce 1994). Institute of Molecular Biology and Biotechnology, Bahauddin Meanwhile, these textile effluents also contain a range of metal Zakariya University, Multan, Pakistan 944 Ann Microbiol (2018) 68:943–952 ions such as cobalt, chromium, manganese, copper, lead, iron, and water resources through different natural and anthropogen- and nickle (Imran et al. 2015a). The ecotoxicological data shows ic processes including mining and smelting activities, combus- that some of the synthetic dyes, aromatic in nature, have been tion of gasoline, sewage sludge, and batteries disposal (Sparks found to be carcinogenic and mutagenic (Ma et al. 2014). Azo 2005; Singh and Gad 2012). The presence of Pb in the natural dyes constitute a key group of synthetic dyes which are exten- media affects plant growth and activity (Sharma and Dubey sively used in textile industries with about 50% share in total 2005) and the microbial communities (Blagodatskaya et al. dyes used worldwide (Stolz 2001;Pandeyet al. 2007). These 2006) including the dye decolorizing bacteria (Hussain et al. are relatively less degradable and, when released along with tex- 2013; Abbas et al. 2016). Hence, the existence of Pb in textile tile effluents, they persist in different components of the environ- wastewaters serves as a hurdle in devising the biological waste- ment including soil and water as a pollutant (Hussain et al. 2013; water treatment technologies involving the use of microbial Loganathan et al. 2015). In soil resources, they do not only populations. In order to cope with this problem, the present disturb the microbial abundance and microbial community struc- study reports the isolation of a Pb tolerant Pseudomonas ture but also have a negative impact on germination and growth aeruginosa strain HF5 which can decolorize different dyes as of plants (Ghodake et al. 2009; Imran et al. 2015a, c). Impact of well as the capability to grow and perform its decolorizing azo dyes to water ecosystem is also largely reported including activity in the presence of considerable concentrations of Pb. esthetic problems, increased chemical oxygen demand (COD), and biological oxygen demand (BOD) and also hindering the light penetration thus ultimately decreasing the activity of aquatic Material and methods life (Chacko and Subramaniam 2011; Imran et al. 2015a). Few azo dyes and their degradation metabolites have also been found Dyes, chemicals, and media to harbor carcinogenic and mutagenic properties having different negative impacts on health of living organisms including human The textile dyes for this study were purchased from Santa Cruz beings (Chacko and Subramaniam 2011; Imran et al. 2015a). In Biotechnology (Shanghai, China). General characteristics includ- order to cope with the harmful effects attributed towards azo ing chemical formula, molecular weight, color index number, dyes, devising the strategies for their remediation from different and wavelength of maximum absorption (λ ) of the dyes used max components of the environment is a topic of interest for the in this study have been presented in Table 1. All other chemicals global scientific communities. and reagents were also of analytical grade and purchased from Recently, the use of potential microbial bioresources for re- Sigma-Aldrich. A mineral salt (MS) medium [composition −1 mediation of azo dyes from the synthetic and real textile waste- (g L ): 1.0 NaCl, 0.1 CaCl .2H O, 0.5 MgSO .7H O, 1.0 2 2 4 2 waters has been reported as an efficient environmental friendly KH PO ,1.0K HPO , 3.0 yeast extract] having 7.2 pH and 2 4 2 4 −1 approach worldwide (Imran et al. 2015a; Maqbool et al. 2016; containing 200 mg L of reactive red-120 (RR120) dye and −1 Hussain et al. 2017). For this purpose, different bacteria from a 50 mg L of Pb as Pb (NO ) was used to isolate lead resistance 3 2 range of genera comprising Comamonas, Shewanella, dye decolorizing bacteria. Whenever required, standard HCl or Pseudomonas, Acinetobacter, Psychrobacter, Serratia, NaOH were used to adjust the pH of the MS medium. Nutrient −1 Enterococcus, Bacillus, Staphylococcus, Proteus,and agar (NA) medium [composition (g L ): 5.0 NaCl, 5.0 peptone, Providencia isolated from different sources have been described 2.0 yeast extract, 15.0 agar] was used to estimate the minimum for biodecolorization of various dyes in synthetic and real textile inhibitory concentration (MIC) of Pb and other metals for HF5 wastewaters (Kalme et al. 2007; Bafana et al. 2009; Bayoumi and other isolates as well as for estimation of population density et al. 2010; Phugare et al. 2011; Khalid et al. 2012;Hussain etal. of the strain HF5 at various pH levels. 2013; Anwar et al. 2014; Imran et al. 2015b; Najme et al. 2015; Abbas et al. 2016; Mahmood et al. 2017). However, it has been Isolation of Pb tolerant strain HF5 observed that growth as well as the decolorizing activity of such strains is affected when the media are amended with various For isolation of Pb tolerant RR120 decolorizing strain, the heavy metal ions individually or in mixtures (Hussain et al. textile wastewater samples were collected from effluent dis- 2013; Imran et al. 2015b;Abbas etal. 2016). Henceforth, the charge sites of various textile industries in Faisalabad bacterial strains with potential of simultaneously decolorizing the (Table S1). The wastewater samples were analyzed for EC azo dyes and resisting various metal ions are needed to be iso- and pH by using Microprocessor Conductivity Model DDS- lated and characterized for their potentials. 120 W and pH meter (Model 1770 D) respectively (Table S1). Lead (Pb) is one of the heavy metal ions often found in Isolation of Pb tolerant RR120 decolorizing bacterial strain textile effluents originating from different textile industries was done through enrichment culture technique using the −1 due to their use in producing pigments for textile dyeing MS broth containing 50 mg L of Pb as Pb (NO ) and 3 2 −1 (Halimoon and Yin 2010; Das et al. 2011). In addition to its 200 mg L of RR120 dye followed by dilution plating. release from textile industries, Pb is also contributed in the soils Enrichment was carried out by inoculating each wastewater Ann Microbiol (2018) 68:943–952 945 −1 Table 1 Decolorization of different azo dyes by Pseudomonas aeruginosa strain HF5 in the liquid media containing 100 mg L of lead (Pb) Dyes Physicochemical characteristics Color removal % Molecular formula Molecular weight Color index no. λ 24 h 48 h 96 h max Reactive Black-5 C H N Na O S 991.80 20,505 597 23.7 ± 3.8 67.4 ± 2.4 71.5 ± 4.8 26 21 5 4 19 6 Reactive Orange-16 C H N Na O S 617.54 17,757 494 81.9 ± 2.5 90.7 ± 3.4 92.4 ± 3.3 20 17 3 2 11 3 Reactive Red-120 C C H N Na O S 1469.98 292,775 535 92.1 ± 4.2 95.7 ± 3.3 96.6 ± 1.9 44 l2 24 14 6 20 6 Reactive Yellow-2 C H C N Na O S 872.96 18,972 404 45.9 ± 5.2 75.8 ± 2.1 83.6 ± 3.5 25 15 l3 9 3 10 3 Direct red-28 C H N Na O S 969.66 22,120 497 19.7 ± 2.9 62.8 ± 7.0 94.5 ± 5.7 32 22 6 2 6 2 individually into MS broth media (1:10 ratio) added with Pb Pb MIC value was chosen for the upcoming experiments. The and RR120, The enrichment cultures along with their respec- isolate HF5 was again tested for decolorization of RR120 tive un-inoculated control were incubated under static condi- under the same conditions and the decolorization was con- tion at 30 °C in dark. After 72 h incubation, decolorization (%) firmed by taking the UV-visible spectra (350–625 nm) of the was examined by comparing the absorbance of aliquots of culture media before and after the decolorization. decolorized media and controls after centrifugation (6000 rpm for 5 min) by UV-visible spectrophotometer Amplification, sequencing, and analyses of 16S rRNA (Shimadzu) at 540 nm (λ ) using the following formula: max of HF5 ðÞ I−F In order to identify HF5, its 16S rRNAwas amplified, sequenced, Decolorization efficiencyðÞ % ¼  100 and analyzed through bioinformatics tools. 16S rRNA sequence was amplified, verified, and purified following the method as where I and F represent the absorbance of the MS broth already described by Maqbool et al. (2016). Sequencing of media before (initial) and after (final) incubation, respectively. 16SrRNA of HF5 was carried out by Macrogen (Seol, South Once more than half of the initially added color was removed, Korea) and the sequence was deposited in Genbank database the cultures from the first enrichment were added to next batch under accession number KF730788. Comparison of this se- of fresh MS amended with RR120 and Pb in 1:10 ration and quence with other known sequences was carried out using the treated up to decolorization in the same way as mentioned program BlastN (https://blast.ncbi.nlm.nih.gov/Blast.cgi). This before. After 4–5 of such cycles, 0.1 mL from each culture sequence was also analyzed through multiple alignments was inoculated on MS + Pb + RR120 agar plates and incubat- followed by the construction of a neighbor joining ed in dark for 48 h at 30 °C. After the incubation, 82 fast- phylogenetic tree as already described by Maqbool et al. (2016). growing bacterial colonies with morphological differences were picked and repeatedly streaked on MS agar media plates Metal tolerance of HF5 for purification. The purified bacterial colonies were screened for their potential to decolorize RR120 in MS broth medium The metal tolerance in terms of minimum inhibitory concentra- containing Pb. For screening, the purified 82 bacterial isolates -I tion (MIC) of the selected heavy metals (Cr, Co, Pb, Zn, Cd, Cu) were allowed to grow in nutrient broth added with 50 mg L for Pseudomonas aeruginosa strain HF5 was assessed in general of Pb as Pb (NO ) . The growth of each isolate was monitored 3 2 purpose medium (GPM) plates by allowing it to grow in the by estimating their optical density (OD ) and homogenized presence of various concentrations of the individual heavy metal to 0.5 OD by adding the fresh medium. Two milliliters of each ions separately at 30 °C (Table S2). The growth of HF5 was culture was inoculated separately in triplicates of 18 mL of -I examined and the concentration of the metal ion at which growth freshly prepared MS broth media containing Pb (50 mg L ) -I of HF5 was halted was considered as MIC of that metal. and RR120 (50 mg L ) and incubated statically along with un- inoculated controls at 30 °C. After 48 h, aliquots from all cultures were centrifuged (6000 rpm for 5 min) and the cell Estimation of decolorization potential of HF5 free extracts were examined for RR120 decolorization. The under varying cultural and incubation conditions isolates having the potential to decolorize RR120 (> 5.0%) were allowed to grow on NA plates added with varying con- Impact of Pb concentration on FH5 growth and RR120 -I centrations (10 to 500 mg L ) of Pb and the minimum inhib- decolorization by HF5 itory concentration (MIC) values of Pb were estimated for the isolates. On the basis of these analyses, the isolate HF5 show- In order to evaluate the impact of varying levels of Pb on ing the maximum RR120 decolorization and a considerable growth of HF5, this strain was allowed to grow separately 946 Ann Microbiol (2018) 68:943–952 under shaking (150 rpm) in different nutrient broth media selected azo dye separately. Triplicates of the MS broth media flasks amended with varying concentrations (0, 100, 200, with various azo dyes were inoculated with strain HF5 (to −1 500 mg L ) of Pb. After 72 h incubation, the HF5 growth develop an initial OD of 0.5) and incubated statically at was assessed in terms of optical density (OD ). Moreover, 30 °C. Respective controls without inoculation were also in- −1 decolorization of RR120 (200 mg L )by Pseudomonas cubated with the samples. Aliquots from triplicate samples of aeruginosa strain HF5 was also evaluated in the presence of each dye were centrifuged (6000 rpm for 5 min) and evaluated −1 various concentrations (0–2000 mg L )ofPb inMS broth for decolorization by taking the absorbance for each dye at media. HF5 cells grown in nutrient broth medium were cen- their respective λ using a UV-visible spectrophotometer. max trifuged at 6000 rpm for 5 min, washed thrice with distilled water, and inoculated (to produce an initial OD of 0.5) in Statistical analyses −1 MS broth media amended with RR120 (200 mg L )and varying levels of Pb. Triplicates of each culture along with The acquired data was analyzed statically by using JMP8® triplicates of un-inoculated controls were incubated statically (SAS Institute Inc., SAS Campus Drive, NC, USA). Wherever at 30 °C. After 48 h incubation, aliquots from all cultures were needed, analyses of variance (ANOVA) were carried out to centrifuged at 6000 rpm for 5 min and cell free extracts were statistically compare the obtained data. then used for estimating the RR120 decolorization as already described above. On the basis of this study, the media used in −1 the rest of experiments were amended with 100 mg L of Pb. Results Effect of pH on RR120 decolorization by HF5 Isolation, screening, and identification of HF5 Potential of Pseudomonas aeruginosa strain HF5 to decolor- While isolating the strain HF5, total 82 purified bacterial col- −1 ize RR120 (200 mg L ) in MS broth media amended with Pb onies were screened for RR120 decolorization. Out of the 82 −1 (100 mg L ) was also examined at five different levels of pH. isolates, only 30 isolates showed the potential to decolorize (> −1 The MS broth media containing RR120 and Pb were adjusted 5%) RR120 in the media containing 50 mg L of Pb (Fig. 1a). at various pH values (5.5, 6.5, 7.5, 8.5, and 9.5) using 0.05 M A huge variation in the decolorization of RR120 by different HCl and 0.05 M NaOH solutions. Triplicate sets of the media isolates was observed in this study. Over 48 h incubation, at each pH were inoculated (to develop an initial OD of 0.1) average decolorization of RR120 by all the isolates was with pre-grown culture of HF5 and incubated statically at 40.1% with the isolate HF18 showing the lowest decoloriza- 30 °C. A triplicate set of un-inoculated media was also incu- tion (5.1 ± 1.3%) and the isolate HF5 showing the highest bated as control along with these samples. At the end of this decolorization (93.5 ± 1.9%). Like RR120 decolorization, −6 experiment, 0.1 mL of the diluted (up to 10 )cultures were the MIC values of Pb for the same 30 bacterial isolates were plated separately on NA plates and incubated at 30 °C. The also found to be variable (Fig. 1b). Most of the isolates were −1 colony forming units (cfu) were counted for each plate. observed to tolerate Pb up to 200 mg L concentration. The highest value of Pb MIC was observed for the isolates HF5 Effect of NaCl concentrations on RR120 decolorization by HF5 and HF29. On the basis of RR120 decolorization and Pb tol- erance, the isolate HF5 was selected for further studies. 16S −1 Decolorization of RR120 (200 mg L ) by HF5 was also eval- rRNA gene sequence of HF5 was deposited in the NCBI −1 uated in the presence of different concentrations (0 g L , GeneBank (GeneBank Ac. No. KF730788). On the basis of −1 −1 −1 −1 10 g L ,20 gL ,50 gL , and 100 g L )ofNaClinMS its identity (> 99%) through BlastN analyses, the strain HF5 −1 brothmedia addedwith 100mgL of Pb. Triplicates of tubes was found belonging to genus Pseudomonas aeruginosa. containing MS broth media with varying levels of NaCl were Moreover, affiliation of this strain with Pseudomonas inoculated with HF5 (to develop an initial OD of 0.5) and aeruginosa was further strengthened on the basis of its group- incubated statically at 30 °C. Over the incubation period, ali- ing in phylogenetic tree with the bacteria of genus quots from each culture were drawn and processed for estimat- Pseudomonas having closest grouping with Pseudomonas ing the decolorization of RR120 as described earlier. aeruginosa strain BCH (Genbank Ac. No. FJ496659) (Fig. 2). On the basis of these analyses, the isolate HF5 was Potential of HF5 for decolorization of various azo dyes named as Pseudomonas aeruginosa strain HF5. Pseudomonas aeruginosa strain HF5 was also tested for its Tolerance of HF5 against Pb and other metals potential of decolorizing various azo dyes including RY2, RB5, RR120, RO16, and DR28 in MS broth media containing Estimation of MIC of different heavy metal ions against the −1 −1 100 mg L of Pb and amended with 200 mg L of each strain HF5 indicated that this strain had the potential to tolerate Ann Microbiol (2018) 68:943–952 947 −1 Fig. 1 a Decolorization of reactive red 120 by the selected bacterial isolates in the presence of 50 mg L of lead (Pb) after 48 h, b minimum inhibitory concentration (MIC) of Pb for the selected bacterial isolates −1 −1 variable levels of different metal ions (Table S2). The MIC 222mgL ),and7.5mM (~843mgL ), respectively. The values of strain HF5 for the different metals including cobalt, resistance of HF5 against the presence of Pb was also estimated chromium, zinc, lead, copper, and cadmium were recorded as by allowing this strain to grow in the presence of different −1 −1 10 mM (~ 590 mg L ), 0.5mM(~26mgL ), 20.0 mM (~ concentrations of Pb. The strain HF5 exhibited a good growth −1 −1 −1 1310 mg L ), 2.75 mM (~ 570 mg L ), 3.5 mM (~ in nutrient broth medium containing 100 mg L of Pb (Fig. 3). 948 Ann Microbiol (2018) 68:943–952 Fig. 2 Neighbor-joining phylogenetic analysis resulting from the GenBank database, used for phylogenetic analysis, are given in multiple alignment of 16S rRNA gene sequence of Pseudomonas brackets. Bootstrap values greater than 800‰ are marked as black aeruginosa strain HF5 with those of other bacterial strains found in the circles and the phylogenetic distance is shown on a scale bar GenBank database. The accession numbers of the strains from the −1 Upon 500 mg L of Pb treatment to nutrient broth medium, the RR120 decolorization at each level with 88.2, 74.3, and growth was found to be significantly reduced which was later 57.5% decolorization of RR120, respectively. −1 reached to the minimum with the 500 mg L of Pb. Under the conditions set in this study, the strain HF5 car- ried out the maximum decolorization in the media whose pH Characterization of the decolorizing capabilities was adjusted at 7.5 and 8.5, respectively (Fig. 5a). Over 24 h of HF5 incubation, this strain decolorized 90.9% and 82.5% of the initially added RR120 at pH values of 7.5 and 8.5, respective- ly. However, over the same incubation period, only 34.8, 43.3, While studying the decolorization of RR120 by HF5 in the media amended with different concentrations of Pb, it was and 43.5% decolorization was observed at pH 5.5, 6.5, and observed that HF5 showed almost complete (> 95%) and sta- 9.5, respectively. Similarly, over 48 h incubation, this strain tistically at par decolorization of RR120 in the media added decolorized 92.8% and 90.6% of the initially added RR120 at −1 with 0, 50, and 100 mg L of Pb (Fig. 4). However, when the pH values of 7.5 and 8.5, respectively. However, over this concentration of Pb was increased up to 500, 1000, and incubation period, 70.3, 74.2, and 76.2% of the initially added −1 2000 mg L , it resulted into a significant reduction in RR120 decolorized at pH 5.5, 6.5, and 9.5, respectively. Fig. 3 Growth of Pseudomonas aeruginosa strain HF5 in nutrient broth medium in the presence of different concentrations of lead (Pb). Filled circles:no Pb (control), filled squares: −1 100 mg L Pb, filled triangles: −1 −1 200 mg L Pb, times: 500 mg L Pb Ann Microbiol (2018) 68:943–952 949 Fig. 4 Decolorization of reactive A 2 per. Mov. Avg. (48 h) red 120 by Pseudomonas aeruginosa strain HF5 in the presence of different lead (Pb) concentrations after 48 h. The different letters on the bars (A, B, C, and D) represent the significant difference between the treatment means 0 mg/L 50 mg/L 100 mg/L 500 mg/L 1000 mg/L 2000 mg/L Lead (Pb) concnetraon Fig. 5 a Effect of pH on the a 24 h 48 h Poly. (24 h) Poly. (48 h) decolorization of reactive red 120 by Pseudomonas aeruginosa strain HF5inliquidculture 90 −1 containing 100 mg L of lead 80 B (Pb). Error bars indicate standard error (n = 3) while the letters indicate the statistical significance. b Correlation between the rate of decolorization 50 B −1 (% h ) and the number of Pseudomonas aeruginosa strain HF5 colonies enumerated on nutrient agar medium −1 (CFU mL ) after their incubation at different pH values. Poly. (24 h) and Poly. (48 h) represent the polynomial curves at 24 and 48 h indicating the trend of decolori- pH 5.5 pH 6.5 pH 7.5 pH 8.5 pH 9.5 zation at varying pH values. The pH different letters on the bars (A and 4.0 B) represent the significant dif- ference between the treatment means pH 7.5 3.5 pH 8.5 3.0 2.5 y = 0.01x + 0.6426 R² = 0.9215 2.0 pH 6.5 pH 9.5 pH 5.5 1.5 1.0 0 50 100 150 200 250 300 350 6 -1 Populaon density (10 CFU mL ) Decolorizaon (%) -1 Rate of decolorizaon (%.h ) Decolorizaon (%) 950 Ann Microbiol (2018) 68:943–952 Similar to the decolorization (%), the cfu values for HF5 were In this study, 30 out of the total 82 purified bacterial colonies similarly higher in the media at pH values of 7.5 and 8.5 as isolated from textile effluents were found to harbor highly var- compared to that of in the media at pH values 5.5, 6.5, and 9.5. iable (from 5.1 to 93.5%) potential to decolorize RR120 in the −1 −1 At varying pH values, the rate of decolorization (% h )was presence of 50 mg L of Pb. Moreover, on the basis of MIC found to be significantly correlated (R of 0.9215) with the values of Pb, these 30 isolates also showed enormous variability growth (cfu) of HF5 (Fig. 5b). in tolerance against the presence of Pb. This finding indicates While evaluating decolorization of RR120 in the presence that different bacterial isolates have a varying potential to resist −1 of different levels of NaCl (0 to 100 g L ) in MS broth media thepresenceofPbaswellasadifferential potential or adaptabil- −1 added with Pb (100 mg L ), it was interestingly found that ity for decolorization of RR120 dye in the media containing Pb. this strain almost completely (> 95%) decolorized RR120 in Suchvariationindecolorizationactivitybydifferent microbial −1 the media having 0, 10, and 20 g L of NaCl (Fig. 6). strains has also been reported by several researchers working on Nevertheless, 77.9% and 27.5% of the added RR120 was microbial decolorization of various dyes (Pandey et al. 2007; found to undergo decolorization when the media were added Lin et al. 2010;Hussain etal. 2013; Anwar et al. 2014; −1 with 50 and 100 g L of NaCl, respectively. Maqbool et al. 2016). Among the various studied bacteria, Besides decolorizing the RR120, the ability of Pseudomonas HF5 strain showed a great potential to grow and decolorizing aeruginosa strain HF5 to decolorize various structurally related the RR120 in media having Pb. This decolorizing ability was azo dyes was also investigated. Results suggested that further tested and verified on UV-visible spectrophotometer Pseudomonas aeruginosa strain HF5 effectively decolorized (350–650 nm) by analyzing the media before and after RR120 all the mentioned reactive dyes and direct dye (Table 1). The decolorization (Fig. S1). On the basis of its 16S rRNA sequence, decolorization of DR28, RB5, RY2, RO16, and RR120 by the it was designated as Pseudomonas aeruginosa strain HF5. Few strain HF5 was recorded to be 19.7 ± 2.9%, 23.7 ± 3.8%, 45.9 ± Pseudomonas aeruginosa strains having the ability to decolorize 5.2%, 81.9 ± 2.5%, and 92.1 ± 4.2%, respectively, over 24 h different azo dyes are previously reported and their decolorizing incubation. However, over 48- and 96-h incubation, the most potential has also been described (Kalme et al. 2007; Joe et al. of all the dyes was decolorized by HF5. 2011; Maqbool et al. 2016). In contrast, the strain HF5 has shown the ability to grow and decolorize the azo dyes even in the presence of considerable concentrations of Pb. In addition to Discussion Pb, this strain also showed a good tolerance in terms of MIC towards the presence of few other metal ions including Co, Cr, Presence of metal ions including lead (Pb) along with the azo Zn, Cu, and Cd in the medium which shows a good potential of dyes in textile wastewaters has a negative impact on living this strain to resist the metal ions which are extensively found in organisms including the microbial populations involved in textile wastewaters. From this information, it can be inferred that decolorization of dyes and create problems while devising this strain can be exploited for removal of dyes even in the wastewaters loaded with heavy metal ions. Such metal tolerance the strategies for bioremediation of such textile wastewaters. This article reports the isolation and characterization of a Pb has also been previously reported in few bacteria having the tolerant Pseudomonas aeruginosa strain HF5 for decoloriza- capability of decolorizing different dyes (Hussain et al. 2013; tion of different azo dyes. Abbas et al. 2016;Maqboolet al. 2016). Fig. 6 Effect of different salt concentrations on decolorization of reactive red 120 by Pseudomonas aeruginosa strain 80 HF5 in the liquid media −1 No salt containing 100 mg L of lead (Pb) 10 g/L 20 g/L 50 g/L 100 g/L 0 20406080 100 120 140 160 Time (Hours) Decolorizaon (%) Ann Microbiol (2018) 68:943–952 951 In this study, higher concentrations (500, 1000, and shows that this strain can be exploited for decolorization of −1 2000 mg L ) of Pb resulted into a significant reduction in different azo dyes. RR120 decolorization while the lower concentrations (50 and On the basis of findings of this study, it can be inferred that −1 100 mg L ) did not have any impact on RR120 decolorization the lead (Pb) resistant Pseudomonas aeruginosa strain HF5 by the strain HF5. This suggests that the activity of this strain is might serve as a new potential bioresource which can be not affected at lower concentrations of Pb but affected at higher exploited for devising the strategies for bioremediation of dif- concentrations. It is also supported by few previous findings ferent azo dyes from the textile wastewaters also contaminated which reported that the microbes can resist the presence of Pb with Pb and other metal ions. only up to a certain limit and, when the concentration exceeds Funding This research work was funded by Government College this limit, the Pb become toxic for the same microbes and affects University, Faisalabad, from its own resources under a GCUF2012 grant. their growth and activity (Aktan et al. 2013;Naiketal. 2012). It is also noteworthy that this strain carried out a significant decol- −1 Compliance with ethical standards orization of RR120 also in the presence of 2000 mg L of Pb which indicates for its unique decolorizing capabilities. Conflict of interest The authors declare that they have no conflict of Decolorizing activity of Pseudomonas aeruginosa strain HF5 interest. monitored at varying pH of the media indicated that a pH from neutral to somewhat alkaline is optimal for achieving optimal Research involving human participants and/or animals A statement for −1 research involving human participants and/or animals is not applicable for decolorization of RR120 in the presence of 100 mg L of Pb. this study. This optimal pH for RR120 decolorization by HF5 is not only relevant with the pH value of the environmental samples from Informed consent A statement regarding informed consent is not appli- which it was isolated but also in line with several previous find- cable for this study. ings focused on studying the impacts of pH on bacterial decol- orization of different dyes (Suzuki et al. 2001; Kalme et al. 2007; Yan et al. 2012; Hussain et al. 2013; Anwar et al. 2014). 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Isolation and characterization of a lead (Pb) tolerant Pseudomonas aeruginosa strain HF5 for decolorization of reactive red-120 and other azo dyes

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Springer Journals
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Copyright © 2018 by Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan
Subject
Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
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1590-4261
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1869-2044
DOI
10.1007/s13213-018-1403-6
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Abstract

Presence of heavy metals including lead (Pb) in the textile effluents is a crucial factor affecting the growth and potential of the dye decolorizing bacterial strains. This work was planned to isolate and characterize a bacterial strain exhibiting the potential to decolorize a range of azo dyes as well as the resistance to Pb. In this study, several Pb tolerant bacteria were isolated from effluents of textile industry. These bacterial isolates were screened for their potential of decolorizing the reactive red-120 (RR120) azo dye −1 with presence of Pb (50 mg L ). The most efficient isolate was further characterized for its potential to resist Pb and decolorize different azo dyes under varying cultural and incubation conditions. Out of the total 82 tested bacterial isolates, 30 bacteria were found to have varying potentials to resist the presence of lead (Pb) and carry out decolorization of an azo dye reactive red-120 −1 (RR120) in the medium amended with Pb (50 mg L ). The most efficient selected bacterium, Pseudomonas aeruginosa strain HF5, was found to show a good potential not only to grow in the presence of considerable concentration of Pb but also to decolorize RR120 and other azo dyes in the media amended with Pb. The strain HF5 completely (> 90%) decolorized RR120 in mineral salt −1 −1 medium amended with 100 mg L of Pband20gL NaCl. This strain also considerably (> 50%) decolorized RR120 up to the −1 −1 presence of 2000 mg L of Pband50gL of NaCl but with reduced rate. The optimal decolorization of RR120 by HF5 was −1 achieved when the pH of the Pb amended (100 mg L ) mineral salt media was adjusted at 7.5 and 8.5. Interestingly, this strain also showed the tolerance to a range of metal ions with varying MIC values. The Pseudomonas aeruginosa strain HF5 harboring the unique potentials to grow and decolorize the azo dyes in the presence of Pb is envisaged as a potential bioresource for devising the remediation strategies for treatment of colored textile wastewaters loaded with Pb and other heavy metal ions. . . . . Keywords Pseudomonas aeruginosa Lead (Pb) tolerance Azo dyes decolorization Heavy metal tolerance NaCl resistance Introduction Farhan Hafeez and Huma Farheen contributed equally to this work. Electronic supplementary material The online version of this article Textile effluents are a major source of freshwater pollution which (https://doi.org/10.1007/s13213-018-1403-6) contains supplementary have been reported to have impacts on different ecological com- material, which is available to authorized users. ponents of the environment as well as the human beings (Chequer et al. 2009;Khanand Malik 2014;Guptaetal. 2015; * Sabir Hussain sabirghani@gmail.com Imran et al. 2015a). These impacts are primarily attributed to- wards the occurrence of enormous amounts of synthetic dyes and Department of Environmental Sciences, COMSATS University heavy metals in the textile effluents (Khan and Malik 2014; Islamabad, Abbottabad Campus, Tobe Camp University Road, Imran et al. 2015a). Reports have suggested that an average Abbottabad 22060, Pakistan −1 concentration of dye may exist up to 300 mg L in the effluent Department of Environmental Sciences & Engineering, Government generated from the textile industries (Tony et al. 2009)which is College University, Allama Iqbal Road, Faisalabad 38000, Pakistan −1 less frequent than the 10–250mgL value as reported by Department of Bioinformatics and Biotechnology, Government O’Neill et al. (1999). Literature has reported as high as College University, Allama Iqbal Road, Faisalabad 38000, Pakistan −1 1500 mg L of dyes in some textile effluents (Pierce 1994). Institute of Molecular Biology and Biotechnology, Bahauddin Meanwhile, these textile effluents also contain a range of metal Zakariya University, Multan, Pakistan 944 Ann Microbiol (2018) 68:943–952 ions such as cobalt, chromium, manganese, copper, lead, iron, and water resources through different natural and anthropogen- and nickle (Imran et al. 2015a). The ecotoxicological data shows ic processes including mining and smelting activities, combus- that some of the synthetic dyes, aromatic in nature, have been tion of gasoline, sewage sludge, and batteries disposal (Sparks found to be carcinogenic and mutagenic (Ma et al. 2014). Azo 2005; Singh and Gad 2012). The presence of Pb in the natural dyes constitute a key group of synthetic dyes which are exten- media affects plant growth and activity (Sharma and Dubey sively used in textile industries with about 50% share in total 2005) and the microbial communities (Blagodatskaya et al. dyes used worldwide (Stolz 2001;Pandeyet al. 2007). These 2006) including the dye decolorizing bacteria (Hussain et al. are relatively less degradable and, when released along with tex- 2013; Abbas et al. 2016). Hence, the existence of Pb in textile tile effluents, they persist in different components of the environ- wastewaters serves as a hurdle in devising the biological waste- ment including soil and water as a pollutant (Hussain et al. 2013; water treatment technologies involving the use of microbial Loganathan et al. 2015). In soil resources, they do not only populations. In order to cope with this problem, the present disturb the microbial abundance and microbial community struc- study reports the isolation of a Pb tolerant Pseudomonas ture but also have a negative impact on germination and growth aeruginosa strain HF5 which can decolorize different dyes as of plants (Ghodake et al. 2009; Imran et al. 2015a, c). Impact of well as the capability to grow and perform its decolorizing azo dyes to water ecosystem is also largely reported including activity in the presence of considerable concentrations of Pb. esthetic problems, increased chemical oxygen demand (COD), and biological oxygen demand (BOD) and also hindering the light penetration thus ultimately decreasing the activity of aquatic Material and methods life (Chacko and Subramaniam 2011; Imran et al. 2015a). Few azo dyes and their degradation metabolites have also been found Dyes, chemicals, and media to harbor carcinogenic and mutagenic properties having different negative impacts on health of living organisms including human The textile dyes for this study were purchased from Santa Cruz beings (Chacko and Subramaniam 2011; Imran et al. 2015a). In Biotechnology (Shanghai, China). General characteristics includ- order to cope with the harmful effects attributed towards azo ing chemical formula, molecular weight, color index number, dyes, devising the strategies for their remediation from different and wavelength of maximum absorption (λ ) of the dyes used max components of the environment is a topic of interest for the in this study have been presented in Table 1. All other chemicals global scientific communities. and reagents were also of analytical grade and purchased from Recently, the use of potential microbial bioresources for re- Sigma-Aldrich. A mineral salt (MS) medium [composition −1 mediation of azo dyes from the synthetic and real textile waste- (g L ): 1.0 NaCl, 0.1 CaCl .2H O, 0.5 MgSO .7H O, 1.0 2 2 4 2 waters has been reported as an efficient environmental friendly KH PO ,1.0K HPO , 3.0 yeast extract] having 7.2 pH and 2 4 2 4 −1 approach worldwide (Imran et al. 2015a; Maqbool et al. 2016; containing 200 mg L of reactive red-120 (RR120) dye and −1 Hussain et al. 2017). For this purpose, different bacteria from a 50 mg L of Pb as Pb (NO ) was used to isolate lead resistance 3 2 range of genera comprising Comamonas, Shewanella, dye decolorizing bacteria. Whenever required, standard HCl or Pseudomonas, Acinetobacter, Psychrobacter, Serratia, NaOH were used to adjust the pH of the MS medium. Nutrient −1 Enterococcus, Bacillus, Staphylococcus, Proteus,and agar (NA) medium [composition (g L ): 5.0 NaCl, 5.0 peptone, Providencia isolated from different sources have been described 2.0 yeast extract, 15.0 agar] was used to estimate the minimum for biodecolorization of various dyes in synthetic and real textile inhibitory concentration (MIC) of Pb and other metals for HF5 wastewaters (Kalme et al. 2007; Bafana et al. 2009; Bayoumi and other isolates as well as for estimation of population density et al. 2010; Phugare et al. 2011; Khalid et al. 2012;Hussain etal. of the strain HF5 at various pH levels. 2013; Anwar et al. 2014; Imran et al. 2015b; Najme et al. 2015; Abbas et al. 2016; Mahmood et al. 2017). However, it has been Isolation of Pb tolerant strain HF5 observed that growth as well as the decolorizing activity of such strains is affected when the media are amended with various For isolation of Pb tolerant RR120 decolorizing strain, the heavy metal ions individually or in mixtures (Hussain et al. textile wastewater samples were collected from effluent dis- 2013; Imran et al. 2015b;Abbas etal. 2016). Henceforth, the charge sites of various textile industries in Faisalabad bacterial strains with potential of simultaneously decolorizing the (Table S1). The wastewater samples were analyzed for EC azo dyes and resisting various metal ions are needed to be iso- and pH by using Microprocessor Conductivity Model DDS- lated and characterized for their potentials. 120 W and pH meter (Model 1770 D) respectively (Table S1). Lead (Pb) is one of the heavy metal ions often found in Isolation of Pb tolerant RR120 decolorizing bacterial strain textile effluents originating from different textile industries was done through enrichment culture technique using the −1 due to their use in producing pigments for textile dyeing MS broth containing 50 mg L of Pb as Pb (NO ) and 3 2 −1 (Halimoon and Yin 2010; Das et al. 2011). In addition to its 200 mg L of RR120 dye followed by dilution plating. release from textile industries, Pb is also contributed in the soils Enrichment was carried out by inoculating each wastewater Ann Microbiol (2018) 68:943–952 945 −1 Table 1 Decolorization of different azo dyes by Pseudomonas aeruginosa strain HF5 in the liquid media containing 100 mg L of lead (Pb) Dyes Physicochemical characteristics Color removal % Molecular formula Molecular weight Color index no. λ 24 h 48 h 96 h max Reactive Black-5 C H N Na O S 991.80 20,505 597 23.7 ± 3.8 67.4 ± 2.4 71.5 ± 4.8 26 21 5 4 19 6 Reactive Orange-16 C H N Na O S 617.54 17,757 494 81.9 ± 2.5 90.7 ± 3.4 92.4 ± 3.3 20 17 3 2 11 3 Reactive Red-120 C C H N Na O S 1469.98 292,775 535 92.1 ± 4.2 95.7 ± 3.3 96.6 ± 1.9 44 l2 24 14 6 20 6 Reactive Yellow-2 C H C N Na O S 872.96 18,972 404 45.9 ± 5.2 75.8 ± 2.1 83.6 ± 3.5 25 15 l3 9 3 10 3 Direct red-28 C H N Na O S 969.66 22,120 497 19.7 ± 2.9 62.8 ± 7.0 94.5 ± 5.7 32 22 6 2 6 2 individually into MS broth media (1:10 ratio) added with Pb Pb MIC value was chosen for the upcoming experiments. The and RR120, The enrichment cultures along with their respec- isolate HF5 was again tested for decolorization of RR120 tive un-inoculated control were incubated under static condi- under the same conditions and the decolorization was con- tion at 30 °C in dark. After 72 h incubation, decolorization (%) firmed by taking the UV-visible spectra (350–625 nm) of the was examined by comparing the absorbance of aliquots of culture media before and after the decolorization. decolorized media and controls after centrifugation (6000 rpm for 5 min) by UV-visible spectrophotometer Amplification, sequencing, and analyses of 16S rRNA (Shimadzu) at 540 nm (λ ) using the following formula: max of HF5 ðÞ I−F In order to identify HF5, its 16S rRNAwas amplified, sequenced, Decolorization efficiencyðÞ % ¼  100 and analyzed through bioinformatics tools. 16S rRNA sequence was amplified, verified, and purified following the method as where I and F represent the absorbance of the MS broth already described by Maqbool et al. (2016). Sequencing of media before (initial) and after (final) incubation, respectively. 16SrRNA of HF5 was carried out by Macrogen (Seol, South Once more than half of the initially added color was removed, Korea) and the sequence was deposited in Genbank database the cultures from the first enrichment were added to next batch under accession number KF730788. Comparison of this se- of fresh MS amended with RR120 and Pb in 1:10 ration and quence with other known sequences was carried out using the treated up to decolorization in the same way as mentioned program BlastN (https://blast.ncbi.nlm.nih.gov/Blast.cgi). This before. After 4–5 of such cycles, 0.1 mL from each culture sequence was also analyzed through multiple alignments was inoculated on MS + Pb + RR120 agar plates and incubat- followed by the construction of a neighbor joining ed in dark for 48 h at 30 °C. After the incubation, 82 fast- phylogenetic tree as already described by Maqbool et al. (2016). growing bacterial colonies with morphological differences were picked and repeatedly streaked on MS agar media plates Metal tolerance of HF5 for purification. The purified bacterial colonies were screened for their potential to decolorize RR120 in MS broth medium The metal tolerance in terms of minimum inhibitory concentra- containing Pb. For screening, the purified 82 bacterial isolates -I tion (MIC) of the selected heavy metals (Cr, Co, Pb, Zn, Cd, Cu) were allowed to grow in nutrient broth added with 50 mg L for Pseudomonas aeruginosa strain HF5 was assessed in general of Pb as Pb (NO ) . The growth of each isolate was monitored 3 2 purpose medium (GPM) plates by allowing it to grow in the by estimating their optical density (OD ) and homogenized presence of various concentrations of the individual heavy metal to 0.5 OD by adding the fresh medium. Two milliliters of each ions separately at 30 °C (Table S2). The growth of HF5 was culture was inoculated separately in triplicates of 18 mL of -I examined and the concentration of the metal ion at which growth freshly prepared MS broth media containing Pb (50 mg L ) -I of HF5 was halted was considered as MIC of that metal. and RR120 (50 mg L ) and incubated statically along with un- inoculated controls at 30 °C. After 48 h, aliquots from all cultures were centrifuged (6000 rpm for 5 min) and the cell Estimation of decolorization potential of HF5 free extracts were examined for RR120 decolorization. The under varying cultural and incubation conditions isolates having the potential to decolorize RR120 (> 5.0%) were allowed to grow on NA plates added with varying con- Impact of Pb concentration on FH5 growth and RR120 -I centrations (10 to 500 mg L ) of Pb and the minimum inhib- decolorization by HF5 itory concentration (MIC) values of Pb were estimated for the isolates. On the basis of these analyses, the isolate HF5 show- In order to evaluate the impact of varying levels of Pb on ing the maximum RR120 decolorization and a considerable growth of HF5, this strain was allowed to grow separately 946 Ann Microbiol (2018) 68:943–952 under shaking (150 rpm) in different nutrient broth media selected azo dye separately. Triplicates of the MS broth media flasks amended with varying concentrations (0, 100, 200, with various azo dyes were inoculated with strain HF5 (to −1 500 mg L ) of Pb. After 72 h incubation, the HF5 growth develop an initial OD of 0.5) and incubated statically at was assessed in terms of optical density (OD ). Moreover, 30 °C. Respective controls without inoculation were also in- −1 decolorization of RR120 (200 mg L )by Pseudomonas cubated with the samples. Aliquots from triplicate samples of aeruginosa strain HF5 was also evaluated in the presence of each dye were centrifuged (6000 rpm for 5 min) and evaluated −1 various concentrations (0–2000 mg L )ofPb inMS broth for decolorization by taking the absorbance for each dye at media. HF5 cells grown in nutrient broth medium were cen- their respective λ using a UV-visible spectrophotometer. max trifuged at 6000 rpm for 5 min, washed thrice with distilled water, and inoculated (to produce an initial OD of 0.5) in Statistical analyses −1 MS broth media amended with RR120 (200 mg L )and varying levels of Pb. Triplicates of each culture along with The acquired data was analyzed statically by using JMP8® triplicates of un-inoculated controls were incubated statically (SAS Institute Inc., SAS Campus Drive, NC, USA). Wherever at 30 °C. After 48 h incubation, aliquots from all cultures were needed, analyses of variance (ANOVA) were carried out to centrifuged at 6000 rpm for 5 min and cell free extracts were statistically compare the obtained data. then used for estimating the RR120 decolorization as already described above. On the basis of this study, the media used in −1 the rest of experiments were amended with 100 mg L of Pb. Results Effect of pH on RR120 decolorization by HF5 Isolation, screening, and identification of HF5 Potential of Pseudomonas aeruginosa strain HF5 to decolor- While isolating the strain HF5, total 82 purified bacterial col- −1 ize RR120 (200 mg L ) in MS broth media amended with Pb onies were screened for RR120 decolorization. Out of the 82 −1 (100 mg L ) was also examined at five different levels of pH. isolates, only 30 isolates showed the potential to decolorize (> −1 The MS broth media containing RR120 and Pb were adjusted 5%) RR120 in the media containing 50 mg L of Pb (Fig. 1a). at various pH values (5.5, 6.5, 7.5, 8.5, and 9.5) using 0.05 M A huge variation in the decolorization of RR120 by different HCl and 0.05 M NaOH solutions. Triplicate sets of the media isolates was observed in this study. Over 48 h incubation, at each pH were inoculated (to develop an initial OD of 0.1) average decolorization of RR120 by all the isolates was with pre-grown culture of HF5 and incubated statically at 40.1% with the isolate HF18 showing the lowest decoloriza- 30 °C. A triplicate set of un-inoculated media was also incu- tion (5.1 ± 1.3%) and the isolate HF5 showing the highest bated as control along with these samples. At the end of this decolorization (93.5 ± 1.9%). Like RR120 decolorization, −6 experiment, 0.1 mL of the diluted (up to 10 )cultures were the MIC values of Pb for the same 30 bacterial isolates were plated separately on NA plates and incubated at 30 °C. The also found to be variable (Fig. 1b). Most of the isolates were −1 colony forming units (cfu) were counted for each plate. observed to tolerate Pb up to 200 mg L concentration. The highest value of Pb MIC was observed for the isolates HF5 Effect of NaCl concentrations on RR120 decolorization by HF5 and HF29. On the basis of RR120 decolorization and Pb tol- erance, the isolate HF5 was selected for further studies. 16S −1 Decolorization of RR120 (200 mg L ) by HF5 was also eval- rRNA gene sequence of HF5 was deposited in the NCBI −1 uated in the presence of different concentrations (0 g L , GeneBank (GeneBank Ac. No. KF730788). On the basis of −1 −1 −1 −1 10 g L ,20 gL ,50 gL , and 100 g L )ofNaClinMS its identity (> 99%) through BlastN analyses, the strain HF5 −1 brothmedia addedwith 100mgL of Pb. Triplicates of tubes was found belonging to genus Pseudomonas aeruginosa. containing MS broth media with varying levels of NaCl were Moreover, affiliation of this strain with Pseudomonas inoculated with HF5 (to develop an initial OD of 0.5) and aeruginosa was further strengthened on the basis of its group- incubated statically at 30 °C. Over the incubation period, ali- ing in phylogenetic tree with the bacteria of genus quots from each culture were drawn and processed for estimat- Pseudomonas having closest grouping with Pseudomonas ing the decolorization of RR120 as described earlier. aeruginosa strain BCH (Genbank Ac. No. FJ496659) (Fig. 2). On the basis of these analyses, the isolate HF5 was Potential of HF5 for decolorization of various azo dyes named as Pseudomonas aeruginosa strain HF5. Pseudomonas aeruginosa strain HF5 was also tested for its Tolerance of HF5 against Pb and other metals potential of decolorizing various azo dyes including RY2, RB5, RR120, RO16, and DR28 in MS broth media containing Estimation of MIC of different heavy metal ions against the −1 −1 100 mg L of Pb and amended with 200 mg L of each strain HF5 indicated that this strain had the potential to tolerate Ann Microbiol (2018) 68:943–952 947 −1 Fig. 1 a Decolorization of reactive red 120 by the selected bacterial isolates in the presence of 50 mg L of lead (Pb) after 48 h, b minimum inhibitory concentration (MIC) of Pb for the selected bacterial isolates −1 −1 variable levels of different metal ions (Table S2). The MIC 222mgL ),and7.5mM (~843mgL ), respectively. The values of strain HF5 for the different metals including cobalt, resistance of HF5 against the presence of Pb was also estimated chromium, zinc, lead, copper, and cadmium were recorded as by allowing this strain to grow in the presence of different −1 −1 10 mM (~ 590 mg L ), 0.5mM(~26mgL ), 20.0 mM (~ concentrations of Pb. The strain HF5 exhibited a good growth −1 −1 −1 1310 mg L ), 2.75 mM (~ 570 mg L ), 3.5 mM (~ in nutrient broth medium containing 100 mg L of Pb (Fig. 3). 948 Ann Microbiol (2018) 68:943–952 Fig. 2 Neighbor-joining phylogenetic analysis resulting from the GenBank database, used for phylogenetic analysis, are given in multiple alignment of 16S rRNA gene sequence of Pseudomonas brackets. Bootstrap values greater than 800‰ are marked as black aeruginosa strain HF5 with those of other bacterial strains found in the circles and the phylogenetic distance is shown on a scale bar GenBank database. The accession numbers of the strains from the −1 Upon 500 mg L of Pb treatment to nutrient broth medium, the RR120 decolorization at each level with 88.2, 74.3, and growth was found to be significantly reduced which was later 57.5% decolorization of RR120, respectively. −1 reached to the minimum with the 500 mg L of Pb. Under the conditions set in this study, the strain HF5 car- ried out the maximum decolorization in the media whose pH Characterization of the decolorizing capabilities was adjusted at 7.5 and 8.5, respectively (Fig. 5a). Over 24 h of HF5 incubation, this strain decolorized 90.9% and 82.5% of the initially added RR120 at pH values of 7.5 and 8.5, respective- ly. However, over the same incubation period, only 34.8, 43.3, While studying the decolorization of RR120 by HF5 in the media amended with different concentrations of Pb, it was and 43.5% decolorization was observed at pH 5.5, 6.5, and observed that HF5 showed almost complete (> 95%) and sta- 9.5, respectively. Similarly, over 48 h incubation, this strain tistically at par decolorization of RR120 in the media added decolorized 92.8% and 90.6% of the initially added RR120 at −1 with 0, 50, and 100 mg L of Pb (Fig. 4). However, when the pH values of 7.5 and 8.5, respectively. However, over this concentration of Pb was increased up to 500, 1000, and incubation period, 70.3, 74.2, and 76.2% of the initially added −1 2000 mg L , it resulted into a significant reduction in RR120 decolorized at pH 5.5, 6.5, and 9.5, respectively. Fig. 3 Growth of Pseudomonas aeruginosa strain HF5 in nutrient broth medium in the presence of different concentrations of lead (Pb). Filled circles:no Pb (control), filled squares: −1 100 mg L Pb, filled triangles: −1 −1 200 mg L Pb, times: 500 mg L Pb Ann Microbiol (2018) 68:943–952 949 Fig. 4 Decolorization of reactive A 2 per. Mov. Avg. (48 h) red 120 by Pseudomonas aeruginosa strain HF5 in the presence of different lead (Pb) concentrations after 48 h. The different letters on the bars (A, B, C, and D) represent the significant difference between the treatment means 0 mg/L 50 mg/L 100 mg/L 500 mg/L 1000 mg/L 2000 mg/L Lead (Pb) concnetraon Fig. 5 a Effect of pH on the a 24 h 48 h Poly. (24 h) Poly. (48 h) decolorization of reactive red 120 by Pseudomonas aeruginosa strain HF5inliquidculture 90 −1 containing 100 mg L of lead 80 B (Pb). Error bars indicate standard error (n = 3) while the letters indicate the statistical significance. b Correlation between the rate of decolorization 50 B −1 (% h ) and the number of Pseudomonas aeruginosa strain HF5 colonies enumerated on nutrient agar medium −1 (CFU mL ) after their incubation at different pH values. Poly. (24 h) and Poly. (48 h) represent the polynomial curves at 24 and 48 h indicating the trend of decolori- pH 5.5 pH 6.5 pH 7.5 pH 8.5 pH 9.5 zation at varying pH values. The pH different letters on the bars (A and 4.0 B) represent the significant dif- ference between the treatment means pH 7.5 3.5 pH 8.5 3.0 2.5 y = 0.01x + 0.6426 R² = 0.9215 2.0 pH 6.5 pH 9.5 pH 5.5 1.5 1.0 0 50 100 150 200 250 300 350 6 -1 Populaon density (10 CFU mL ) Decolorizaon (%) -1 Rate of decolorizaon (%.h ) Decolorizaon (%) 950 Ann Microbiol (2018) 68:943–952 Similar to the decolorization (%), the cfu values for HF5 were In this study, 30 out of the total 82 purified bacterial colonies similarly higher in the media at pH values of 7.5 and 8.5 as isolated from textile effluents were found to harbor highly var- compared to that of in the media at pH values 5.5, 6.5, and 9.5. iable (from 5.1 to 93.5%) potential to decolorize RR120 in the −1 −1 At varying pH values, the rate of decolorization (% h )was presence of 50 mg L of Pb. Moreover, on the basis of MIC found to be significantly correlated (R of 0.9215) with the values of Pb, these 30 isolates also showed enormous variability growth (cfu) of HF5 (Fig. 5b). in tolerance against the presence of Pb. This finding indicates While evaluating decolorization of RR120 in the presence that different bacterial isolates have a varying potential to resist −1 of different levels of NaCl (0 to 100 g L ) in MS broth media thepresenceofPbaswellasadifferential potential or adaptabil- −1 added with Pb (100 mg L ), it was interestingly found that ity for decolorization of RR120 dye in the media containing Pb. this strain almost completely (> 95%) decolorized RR120 in Suchvariationindecolorizationactivitybydifferent microbial −1 the media having 0, 10, and 20 g L of NaCl (Fig. 6). strains has also been reported by several researchers working on Nevertheless, 77.9% and 27.5% of the added RR120 was microbial decolorization of various dyes (Pandey et al. 2007; found to undergo decolorization when the media were added Lin et al. 2010;Hussain etal. 2013; Anwar et al. 2014; −1 with 50 and 100 g L of NaCl, respectively. Maqbool et al. 2016). Among the various studied bacteria, Besides decolorizing the RR120, the ability of Pseudomonas HF5 strain showed a great potential to grow and decolorizing aeruginosa strain HF5 to decolorize various structurally related the RR120 in media having Pb. This decolorizing ability was azo dyes was also investigated. Results suggested that further tested and verified on UV-visible spectrophotometer Pseudomonas aeruginosa strain HF5 effectively decolorized (350–650 nm) by analyzing the media before and after RR120 all the mentioned reactive dyes and direct dye (Table 1). The decolorization (Fig. S1). On the basis of its 16S rRNA sequence, decolorization of DR28, RB5, RY2, RO16, and RR120 by the it was designated as Pseudomonas aeruginosa strain HF5. Few strain HF5 was recorded to be 19.7 ± 2.9%, 23.7 ± 3.8%, 45.9 ± Pseudomonas aeruginosa strains having the ability to decolorize 5.2%, 81.9 ± 2.5%, and 92.1 ± 4.2%, respectively, over 24 h different azo dyes are previously reported and their decolorizing incubation. However, over 48- and 96-h incubation, the most potential has also been described (Kalme et al. 2007; Joe et al. of all the dyes was decolorized by HF5. 2011; Maqbool et al. 2016). In contrast, the strain HF5 has shown the ability to grow and decolorize the azo dyes even in the presence of considerable concentrations of Pb. In addition to Discussion Pb, this strain also showed a good tolerance in terms of MIC towards the presence of few other metal ions including Co, Cr, Presence of metal ions including lead (Pb) along with the azo Zn, Cu, and Cd in the medium which shows a good potential of dyes in textile wastewaters has a negative impact on living this strain to resist the metal ions which are extensively found in organisms including the microbial populations involved in textile wastewaters. From this information, it can be inferred that decolorization of dyes and create problems while devising this strain can be exploited for removal of dyes even in the wastewaters loaded with heavy metal ions. Such metal tolerance the strategies for bioremediation of such textile wastewaters. This article reports the isolation and characterization of a Pb has also been previously reported in few bacteria having the tolerant Pseudomonas aeruginosa strain HF5 for decoloriza- capability of decolorizing different dyes (Hussain et al. 2013; tion of different azo dyes. Abbas et al. 2016;Maqboolet al. 2016). Fig. 6 Effect of different salt concentrations on decolorization of reactive red 120 by Pseudomonas aeruginosa strain 80 HF5 in the liquid media −1 No salt containing 100 mg L of lead (Pb) 10 g/L 20 g/L 50 g/L 100 g/L 0 20406080 100 120 140 160 Time (Hours) Decolorizaon (%) Ann Microbiol (2018) 68:943–952 951 In this study, higher concentrations (500, 1000, and shows that this strain can be exploited for decolorization of −1 2000 mg L ) of Pb resulted into a significant reduction in different azo dyes. RR120 decolorization while the lower concentrations (50 and On the basis of findings of this study, it can be inferred that −1 100 mg L ) did not have any impact on RR120 decolorization the lead (Pb) resistant Pseudomonas aeruginosa strain HF5 by the strain HF5. This suggests that the activity of this strain is might serve as a new potential bioresource which can be not affected at lower concentrations of Pb but affected at higher exploited for devising the strategies for bioremediation of dif- concentrations. It is also supported by few previous findings ferent azo dyes from the textile wastewaters also contaminated which reported that the microbes can resist the presence of Pb with Pb and other metal ions. only up to a certain limit and, when the concentration exceeds Funding This research work was funded by Government College this limit, the Pb become toxic for the same microbes and affects University, Faisalabad, from its own resources under a GCUF2012 grant. their growth and activity (Aktan et al. 2013;Naiketal. 2012). It is also noteworthy that this strain carried out a significant decol- −1 Compliance with ethical standards orization of RR120 also in the presence of 2000 mg L of Pb which indicates for its unique decolorizing capabilities. Conflict of interest The authors declare that they have no conflict of Decolorizing activity of Pseudomonas aeruginosa strain HF5 interest. monitored at varying pH of the media indicated that a pH from neutral to somewhat alkaline is optimal for achieving optimal Research involving human participants and/or animals A statement for −1 research involving human participants and/or animals is not applicable for decolorization of RR120 in the presence of 100 mg L of Pb. this study. This optimal pH for RR120 decolorization by HF5 is not only relevant with the pH value of the environmental samples from Informed consent A statement regarding informed consent is not appli- which it was isolated but also in line with several previous find- cable for this study. ings focused on studying the impacts of pH on bacterial decol- orization of different dyes (Suzuki et al. 2001; Kalme et al. 2007; Yan et al. 2012; Hussain et al. 2013; Anwar et al. 2014). 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Annals of Microbiology – Springer Journals

Published: Nov 14, 2018

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