Abstract
A psychrotolerant bacterial strain of Pseudomonas sp. (P. palleroniana GBPI_508), isolated from the Indian Himalayan region, is studied for analyzing its potential for degrading bisphenol A (BPA). Response surface methodology using Box–Behnken design was used to statistically optimize the environmental factors during BPA degradation and the maximum degradation (97%) was obtained at optimum conditions of mineral salt media pH 9, experimental temperature 25 °C, an inoculum volume of 10% (v/v), and agitation speed 130 rpm at the BPA concentration 270 mg L−1. The Monod model was used for understanding bacterial degradation kinetics, and 37.5 mg−1 half saturation coefficient (KS) and 0.989 regression coefficient (R2) were obtained. Besides, the utmost specific growth rate µmax was witnessed as 0.080 h−1 with the GBPI_508 during BPA degradation. Metabolic intermediates detected in this study by GC–MS were identified as valeric acid, propionic acid, diglycolic acid, and phenol. The psychrotolerant bacterial strain of Pseudomonas sp. (P. palleroniana GBPI_508), isolated from the Indian Himalayan region has shown good potential for remediation of BPA at variable conditions.
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References
Almeida S, Raposo A, Almeida-González M, Carrascosa C (2018) Bisphenol A: food exposure and impact on human health. Compr Rev Food Sci Food Saf 17:1503–1517. https://doi.org/10.1111/1541-4337.12388
Annuar MSM, Tan IKP, Ibrahim S, Ramachandran KB (2008) A kinetic model for growth and biosynthesis of medium-chain-length poly-(3 -hydroxyalkanoates) in Pseudomonas putida. Braz J Chem Eng 25:217–228. https://doi.org/10.1590/S0104-66322008000200001
Badiefar L, Yakhchali B, Rodriguez-Couto S, Veloso A, García-Arenzana JM, Matsumura Y, Khodabandeh M (2015) Biodegradation of bisphenol A by the newly-isolated Enterobacter gergoviae strain BYK-7 enhanced using genetic manipulation. RSC Adv 5:29563–29572. https://doi.org/10.1039/c5ra01818h
Bitton G (1994) Wastewater microbiology. Wiley-Liss Inc., Hoboken
Box GEP, Behnken DW (1960) Some new three level designs for the study of quantitative variables. Technometrics 2:455–475. https://doi.org/10.1080/00401706.1960.10489912
Burhan A, Nisa U, Gökhan C, Ömer C, Ashabil A, Osman G (2003) Enzymatic properties of a novel thermostable, thermophilic, alkaline and chelator resistant amylase from an alkaliphilic Bacillus sp. isolate ANT-6. Process Biochem 38:1397–1403. https://doi.org/10.1016/S0032-9592(03)00037-2
Chai W, Handa Y, Suzuki M, Saito M, Kato N, Horiuchi CA (2005) Biodegradation of bisphenol A by fungi. Appl Biochem Biotechnol 120:175–180. https://doi.org/10.1385/ABAB:120:3:175
Corrales J, Kristofco LA, Baylor Steele W, Yates BS, Breed CS, Spencer Williams E, Brooks BW (2015) Global assessment of bisphenol a in the environment: review and analysis of its occurrence and bioaccumulation. Dose-Response 13:1–29. https://doi.org/10.1177/1559325815598308
Dahiru T (2011) P value, a true test of statistical significance? A cautionary note. Ann Ibadan Postgrad Med 6:21–26. https://doi.org/10.4314/aipm.v6i1.64038
Dhakar K, Pandey A (2016) Wide pH range tolerance in extremophiles: towards understanding an important phenomenon for future biotechnology. Appl Microbiol Biotechnol 100:2499–2510. https://doi.org/10.1007/s00253-016-7285-2
Dhakar K, Pandey A (2020) Microbial ecology from the Himalayan cryosphere perspective. Microorganisms 8:1–17. https://doi.org/10.3390/microorganisms8020257
Eio EJ, Kawai M, Tsuchiya K, Yamamoto S, Toda T (2014) Biodegradation of bisphenol A by bacterial consortia. Int Biodeterior Biodegrad 96:166–173. https://doi.org/10.1016/j.ibiod.2014.09.011
Eltoukhy A, Jia Y, Nahurira R, Abo-Kadoum MA, Khokhar I, Wang J, Yan Y (2020) Biodegradation of endocrine disruptor bisphenol A by Pseudomonas putida strain YC-AE1 isolated from polluted soil, Guangdong. China BMC Microbiol. https://doi.org/10.1186/s12866-020-1699-9
Engqvist MKM (2018) Correlating enzyme annotations with a large set of microbial growth temperatures reveals metabolic adaptations to growth at diverse temperatures 06 biological sciences 0605 microbiology 06 biological sciences 0601 biochemistry and cell biology. BMC Microbiol 18:1–14. https://doi.org/10.1186/s12866-018-1320-7
Ferreira SLC, Bruns RE, Ferreira HS, Matos GD, David JM, Brandão GC, da Silva EGP, Portugal LA, dos Reis PS, Souza AS, dos Santos WNL (2007) Box-Behnken design: an alternative for the optimization of analytical methods. Anal Chim Acta 597:179–186. https://doi.org/10.1016/j.aca.2007.07.011
Flint S, Markle T, Thompson S, Wallace E (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manage 104:19–34. https://doi.org/10.1016/j.jenvman.2012.03.021
Gray RD (1992) The molecular basis of electron transfer in cytochrome P450 enzyme systems. Front Biotransform 7:321–350
Jain R, Pandey A, Pasupuleti M, Pande V (2017) Prolonged production and aggregation complexity of cold-active lipase from Pseudomonas proteolytica (GBPI_Hb61) isolated from cold desert Himalaya. Mol Biotechnol 59:34–45. https://doi.org/10.1007/s12033-016-9989-z
Kamaraj M, Sivaraj R, Venckatesh R (2014) Biodegradation of bisphenol A by the tolerant bacterial species isolated from coastal regions of Chennai, Tamil Nadu, India. Int Biodeterior Biodegrad 93:216–222. https://doi.org/10.1016/j.ibiod.2014.02.014
Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enzyme Res. https://doi.org/10.4061/2011/805187
Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315. https://doi.org/10.1128/mmbr.54.3.305-315.1990
Lee E, Ku S, Jung M, Lee S (2019) Simple and rapid detection of bisphenol A using a gold nanoparticle-based colorimetric aptasensor. Food Chem 287:205–213. https://doi.org/10.1016/j.foodchem.2019.02.079
Li G, Zu L, Wong PK, Hui X, Lu Y, Xiong J, An T (2012) Biodegradation and detoxification of bisphenol A with one newly-isolated strain Bacillus sp. GZB: kinetics, mechanism and estrogenic transition. Bioresour Technol 114:224–230. https://doi.org/10.1016/j.biortech.2012.03.067
Lobos JH, Leib TK, Su TM (1992) Biodegradation of bisphenol A and other bisphenols by a gram-negative aerobic bacterium. Appl Environ Microbiol 58:1823–1831
Malinverno A, Martinez EA (2015) The effect of temperature on organic carbon degradation in marine sediments. Sci Rep 5:1–10. https://doi.org/10.1038/srep17861
Margesin R, Schinner F (1997) Effect of temperature on oil degradation by psychrotrophic yeast in liquid culture and in soil. FEMS Microb Ecol 24:243–249
Masuda M, Yamasaki Y, Ueno S, Inoue A (2007) Isolation of bisphenol A-tolerant/degrading Pseudomonas monteilii strain N-502. Extremophiles 11:355–362. https://doi.org/10.1007/s00792-006-0047-9
Monod J (1949) The growth of bacterial cultures. Ann Rev Microbiol 3(1):371–394
Nicole M, Chamberland H, Geiger JP, Lecours N, Valero J, Rio B, Ouellette GB (1992) Immunocytochemical localization of laccase L1 in wood decayed by Rigidoporus lignosus. Appl Environ Microbiol 58:1727–1739. https://doi.org/10.1128/aem.58.5.1727-1739.1992
Oshiman KI, Tsutsumi Y, Nishida T, Matsumura Y (2007) Isolation and characterization of a novel bacterium, Sphingomonas bisphenolicum strain AO1, that degrades bisphenol A. Biodegradation 18:247–255. https://doi.org/10.1007/s10532-006-9059-5
Pandey A, Jain R, Sharma A, Dhakar K, Kaira GS, Rahi P, Dhyani A, Pandey N, Adhikari P, Shouche YS (2019) 16S rRNA gene sequencing and MALDI-TOF mass spectrometry based comparative assessment and bioprospection of psychrotolerant bacteria isolated from high altitudes under mountain ecosystem. SN Appl Sci 1:278. https://doi.org/10.1007/s42452-019-0273-2
Peng YH, Chen YJ, Chang YJ, Shih YH (2015) Biodegradation of bisphenol A with diverse microorganisms from river sediment. J Hazard Mater 286:285–290. https://doi.org/10.1016/j.jhazmat.2014.12.051
Reardon KF, Mosteller DC, Rogers JB, DuTeau NM, Kim KH (2002) Biodegradation kinetics of aromatic hydrocarbon mixtures by pure and mixed bacterial cultures. Environ Health Perspect 110:1005–1011. https://doi.org/10.1289/ehp.02110s61005
Ronen Z, Abeliovich A (2000) Anaerobic-aerobic process for microbial degradation of tetrabromobisphenol A. Appl Environ Microbiol 66:2372–2377. https://doi.org/10.1128/AEM.66.6.2372-2377.2000
Sakai K, Yamanaka H, Moriyoshi K, Ohmoto T, Ohe T (2007) Biodegradation of bisphenol A and related compounds by Sphingomonas sp. strain BP-7 isolated from seawater. Biosci Biotechnol Biochem 71:51–57. https://doi.org/10.1271/bbb.60351
Sasaki M, Akahira A, Oshiman KI, Tsuchido T, Matsumura Y (2005a) Purification of cytochrome P450 and ferredoxin, involved in bisphenol A degradation, from Sphingomonas sp. strain AO1. Appl Environ Microbiol 71:8024–8030. https://doi.org/10.1128/AEM.71.12.8024-8030.2005
Sasaki M, Maki JI, Oshiman KI, Matsumura Y, Tsuchido T (2005b) Biodegradation of bisphenol A by cells and cell lysate from Sphingomonas sp. strain AO1. Biodegradation 16:449–459. https://doi.org/10.1007/s10532-004-5023-4
Staples CA, Dorn PB, Klecka GM, O’Block ST, Harris LR (1998) A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 36:2149–2173. https://doi.org/10.1016/s0045-6535(97)10133-3
Suyamud B, Inthorn D, Panyapinyopol B, Thiravetyan P (2018a) Biodegradation of Bisphenol A by a newly isolated Bacillus megaterium strain ISO-2 from a polycarbonate industrial wastewater. Water Air Soil Pollut 229:347–359. https://doi.org/10.1007/s11270-018-3983-y
Suyamud B, Inthorn D, Panyapinyopol B, Thiravetyan P (2018b) Biodegradation of bisphenol A by a newly isolated Bacillus megaterium strain ISO-2 from a polycarbonate industrial wastewater. Water Air Soil Pollut 229:348–359. https://doi.org/10.1007/s11270-018-3983-y
Vaidya S, Devpura N, Jain K, Madamwar D (2018) Degradation of chrysene by enriched bacterial consortium. Front Microbiol 9:1–14. https://doi.org/10.3389/fmicb.2018.01333
Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139–177. https://doi.org/10.1016/j.reprotox.2007.07.010
Vijayalakshmi V, Senthilkumar P, Mophin-Kani K, Sivamani S, Sivarajasekar N, Vasantharaj S (2018) Bio-degradation of bisphenol A by Pseudomonas aeruginosa PAb1 isolated from effluent of thermal paper industry: kinetic modeling and process optimization. J Radiat Res Appl Sci 11:56–65. https://doi.org/10.1016/j.jrras.2017.08.003
Wong L-L (1998) Cytochrome P450 monooxygenases. Curr Opin Chem Biol 2:263–268. https://doi.org/10.1101/gad.986602.te
Yamanaka H, Moriyoshi K, Ohmoto T, Ohe T, Sakai K (2008) Efficient microbial degradation of bisphenol A in the presence of activated carbon. J Biosci Bioeng 105:157–160. https://doi.org/10.1263/jbb.105.157
Yu K, Yi S, Li B, Guo F, Peng X, Wang Z, Wu Y (2019) An integrated meta-omics approach reveals substrates involved in synergistic interactions in a bisphenol A (BPA)—degrading microbial community. Microbiome 7:1–13
Zhang C, Zeng G, Yuan L, Yu J, Li J, Huang G, Xi B, Liu H (2007) Aerobic degradation of bisphenol A by Achromobacter xylosoxidans strain B-16 isolated from compost leachate of municipal solid waste. Chemosphere 68:181–190. https://doi.org/10.1016/j.chemosphere.2006.12.012
Acknowledgements
Authors are grateful to the Director GBP-NIHE for extending their facilities and the Department of Science and Technology-Water Technology Initiative (DST-WTI) [DST/TM/WTI/2K15/63C] for financial support. We are also thankful to AIRF-JNU for providing facilities for GC–MS analysis.
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This research work was supported by Department of Science and Technology-Water Technology Initiative, DST/TM/WTI/2K15/63C.
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Thathola, P., Agnihotri, V., Pandey, A. et al. Biodegradation of bisphenol A using psychrotolerant bacterial strain Pseudomonas palleroniana GBPI_508. Arch Microbiol 204, 272 (2022). https://doi.org/10.1007/s00203-022-02885-y
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DOI: https://doi.org/10.1007/s00203-022-02885-y