Abstract
Polychlorinated biphenyls (PCBs) are typical lasting organic pollutants. Persistence and recalcitrance to biodegradation of PCBs have hampered the transformation of PCB congeners from the environment. Biological transformation of polychlorinated biphenyls could take place through anaerobic dechlorination, aerobic microbial degradation, and a combination of transformation of anaerobic dechlorination and aerobic degradation. Under anaerobic conditions, microbial dechlorination is an important degradation mode for PCBs, especially high-chlorinated congeners. The low-chlorinated compounds formed after reductive dechlorination could be further aerobically degraded and completely mineralized. This paper reviews the recent advances in biological degradation of PCBs, introduces the functional bacteria and enzymes involved in the anaerobic and aerobic degradation of PCBs, and discusses the synergistic action of anaerobic reduction and aerobic degradation. In addition, the different ways to the microbial remediation of PCBs-contaminated environments are discussed. This review provides a theoretical foundation and practical basis to use PCBs-degrading microorganisms for bioremediation.
Similar content being viewed by others
References
Adebusoye SA, Ilori MO, Picardal FW, Amund OO (2008) Metabolism of chlorinated biphenyls: use of 3,3'- and 3,5-dichlorobiphenyl as sole sources of carbon by natural species of Ralstonia and Pseudomonas. Chemosphere 70:656–663. https://doi.org/10.1016/j.chemosphere.2007.06.079
Adebusoye SA, Picardal FW, Ilori MO, Amund OO (2008) Evidence of aerobic utilization of di-ortho-substituted trichlorobiphenyls as growth substrates by Pseudomonas sp. SA-6 and Ralstonia sp. SA-4. Environ Microbiol 10:1165–1174. https://doi.org/10.1111/j.1462-2920.2007.01533.x
Adrian L, Dudkova V, Demnerova K, Bedard DL (2009) Dehalococcoides sp. strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl mixture aroclor 1260. Appl Environ Microbiol 75:4516–4524. https://doi.org/10.1128/AEM.00102-09
Bedard DL (2014) PCB dechlorinases revealed at last. Proc Natl Acad Sci USA 111:11919–11920. https://doi.org/10.1073/pnas.1412286111
Bedard DL, Ritalahti KM, Loffler FE (2007) The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture aroclor 1260. Appl Environ Microbiol 73:2513–2521. https://doi.org/10.1128/AEM.02909-06
Cai M, Song G, Li Y, Du K (2018) A novel Aroclor 1242-degrading culturable endophytic bacterium isolated from tissue culture seedlings of Salix matsudana f. pendula Schneid. Phytochem Lett 23:66–72. https://doi.org/10.1016/j.phytol.2017.11.012
Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agullo L, Reyes VL, Hauser L, Cordova L, Gomez L, Gonzalez M, Land M, Lao V, Larimer F, LiPuma JJ, Mahenthiralingam E, Malfatti SA, Marx CJ, Parnell JJ, Ramette A, Richardson P, Seeger M, Smith D, Spilker T, Sul WJ, Tsoi TV, Ulrich LE, Zhulin IG, Tiedje JM (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 103:15280–15287. https://doi.org/10.1073/pnas.0606924103
Chen C, Yu C, Shen C, Tang X, Qin Z, Yang K, Hashmi MZ, Huang R, Shi H (2014) Paddy field-a natural sequential anaerobic-aerobic bioreactor for polychlorinated biphenyls transformation. Environ Pollut 190:43–50. https://doi.org/10.1016/j.envpol.2014.03.018
Elangovan S, Pandian SBS, Geetha SJ, Joshi SJ (2019) Polychlorinated biphenyls (PCBs): environmental fate, challenges and bioremediation. In: Arora PK (ed) Microbial Metabolism of Xenobiotic Compounds. Springer, Singapore, pp 165-188. https://doi.org/10.1007/978-981-13-7462-3_8
Ewald JM, Humes SV, Martinez A, Schnoor JL, Mattes TE (2019) Growth of Dehalococcoides spp. and increased abundance of reductive dehalogenase genes in anaerobic PCB-contaminated sediment microcosms. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-019-05571-7
Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Haggblom MM (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081. https://doi.org/10.1021/es034989b
Field JA, Sierra-Alvarez R (2008) Microbial transformation and degradation of polychlorinated biphenyls. Environ Pollut 155:1–12. https://doi.org/10.1016/j.envpol.2007.10.016
Frederiksen M, Andersen HV, Haug LS, Thomsen C, Broadwell SL, Egsmose EL, Kolarik B, Gunnarsen L, Knudsen LE (2020) PCB in serum and hand wipes from exposed residents living in contaminated high-rise apartment buildings and a reference group. Int J Hyg Environ Health 224:113430. https://doi.org/10.1016/j.ijheh.2019.113430
Furukawa K (1994) Molecular genetics and evolutionary relationship of PCB-degrading bacteria. Biodegradation 5:289–300. https://doi.org/10.1007/bf00696466
Garrido-Sanz D, Sansegundo-Lobato P, Redondo-Nieto M, Suman J, Cajthaml T, Blanco-Romero E, Martin M, Uhlik O, Rivilla R (2020) Analysis of the biodegradative and adaptive potential of the novel polychlorinated biphenyl degrader Rhodococcus sp WAY2 revealed by its complete genome sequence. Microb Genom. https://doi.org/10.1099/mgen.0.000363
Haddock JD, Gibson DT (1995) Purification and characterization of the oxygenase component of biphenyl 2,3-dioxygenase from Pseudomonas sp. strain LB400. J Bacteriol 177:5834–5839. https://doi.org/10.1128/jb.177.20.5834-5839.1995
Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601. https://doi.org/10.1146/annurev.mi.46.100192.003025
Hayat A, Hussain I, Soja G, Iqbal M, Shahid N, Syed JH, Yousaf S (2019) Organic and chemical amendments positively modulate the bacterial proliferation for effective rhizoremediation of PCBs-contaminated soil. Ecol Eng 138:412–419. https://doi.org/10.1016/j.ecoleng.2019.07.038
Hendrickson ER, Payne JA, Young RM, Starr MG, Perry MP, Fahnestock S, Ellis DE, Ebersole RC (2002) Molecular analysis of Dehalococcoides 16S ribosomal DNA from chloroethene-contaminated sites throughout North America and Europe. Appl Environ Microbiol 68:485–495. https://doi.org/10.1128/aem.68.2.485-495.2002
Hirose J, Fujihara H, Watanabe T, Kimura N, Suenaga H, Futagami T, Goto M, Suyama A, Furukawa K (2019) Biphenyl/PCB degrading bph genes of ten bacterial strains isolated from biphenyl-contaminated soil in Kitakyushu, Japan: comparative and dynamic features as integrative conjugative elements (ICEs). Genes 10:404. https://doi.org/10.3390/genes10050404
Hofer B, Backhaus S, Timmis KN (1994) The biphenyl/polychlorinated biphenyl-degradation locus (bph) of Pseudomonas sp. LB400 encodes four additional metabolic enzymes. Gene 144:9–16. https://doi.org/10.1016/0378-1119(94)90196-1
Horváthová H, Lászlová K, Dercová K (2018) Bioremediation of PCB-contaminated shallow river sediments: the efficacy of biodegradation using individual bacterial strains and their consortia. Chemosphere 193:270–277. https://doi.org/10.1016/j.chemosphere.2017.11.012
Hu J, Qian M, Zhang Q, Cui J, Yu C, Su X, Shen C, Hashm MZ, Shi J (2015) Sphingobium fuliginis HC3: a novel and robust isolated biphenyl- and polychlorinated biphenyls-degrading bacterium without dead-end intermediates accumulation. PLoS One 10:e0122740. https://doi.org/10.1371/journal.pone.0122740
Ilori MO, Robinson GK, Adebusoye SA (2008) Degradation and mineralization of 2-chloro-, 3-chloro- and 4-chlorobiphenyl by a newly characterized natural bacterial strain isolated from an electrical transformer fluid-contaminated soil. J Environ Sci (China) 20:1250–1257. https://doi.org/10.1016/s1001-0742(08)62217-2
Jahnke JC, Hornbuckle KC (2019) PCB emissions from paint colorants. Environ Sci Technol 53:5187–5194. https://doi.org/10.1021/acs.est.9b01087
Jing R, Fusi S, Kjellerup BV (2018) Remediation of polychlorinated biphenyls (PCBs) in contaminated soils and sediment: state of knowledge and perspectives. Front Environ Sci 6:79. https://doi.org/10.3389/fenvs.2018.00079
Kikuchi Y, Yasukochi Y, Nagata Y, Fukuda M, Takagi M (1994) Nucleotide sequence and functional analysis of the meta-cleavage pathway involved in biphenyl and polychlorinated biphenyl degradation in Pseudomonas sp. strain KKS102. J Bacteriol 176:4269–4276. https://doi.org/10.1128/jb.176.14.4269-4276.1994
Klocke C, Lein PJ (2020) Evidence implicating non-dioxin-like congeners as the key mediators of polychlorinated biphenyl (PCB) developmental neurotoxicity. Int J Mol Sci. https://doi.org/10.3390/ijms21031013
LaRoe SL, Fricker AD, Bedard DL (2014) Dehalococcoides mccartyi strain JNA in pure culture extensively dechlorinates Aroclor 1260 according to polychlorinated biphenyl (PCB) dechlorination process N. Environ Sci Technol 48:9187–9196. https://doi.org/10.1021/es500872t
Lehtinen T, Mikkonen A, Sigfusson B, Olafsdottir K, Ragnarsdottir KV, Guicharnaud R (2014) Bioremediation trial on aged PCB-polluted soils-a bench study in Iceland. Environ Sci Pollut Res Int 21:1759–1768. https://doi.org/10.1007/s11356-013-2069-z
Liang Y, Meggo R, Hu D, Schnoor JL, Mattes TE (2014) Enhanced polychlorinated biphenyl removal in a switchgrass rhizosphere by bioaugmentation with Burkholderia xenovorans LB400. Ecol Eng 71:215–222. https://doi.org/10.1016/j.ecoleng.2014.07.046
Masai E, Yamada A, Healy JM, Hatta T, Kimbara K, Fukuda M, Yano K (1995) Characterization of biphenyls catabolic genes of gram-positive polychlorinated biphenyls degrader Rhodococcus sp. strain RHA1. Appl Environ Microbiol 61:2079–2085
Matturro B, Di Lenola M, Ubaldi C, Rossetti S (2016) First evidence on the occurrence and dynamics of Dehalococcoides mccartyi PCB-dechlorinase genes in marine sediment during Aroclor1254 reductive dechlorination. Mar Pollut Bull 112:189–194. https://doi.org/10.1016/j.marpolbul.2016.08.021
Matturro B, Ubaldi C, Rossetti S (2016) Microbiome dynamics of a polychlorobiphenyl (PCB) historically contaminated marine sediment under conditions promoting reductive dechlorination. Front Microbiol 7:1502. https://doi.org/10.3389/fmicb.2016.01502
Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Cunha Tarouco P, Weyrauch P, Dong X, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microb Biotech 26:92–118. https://doi.org/10.1159/000441358
Mikeskova H, Novotny C, Svobodova K (2012) Interspecific interactions in mixed microbial cultures in a biodegradation perspective. Appl Microbiol Biotechnol 95:861–870. https://doi.org/10.1007/s00253-012-4234-6
Mizukami-Murata S, Sakakibara F, Fujita K, Fukuda M, Kuramata M, Takagi K (2016) Detoxification of hydroxylated polychlorobiphenyls by Sphingomonas sp. strain N-9 isolated from forest soil. Chemosphere 165:173–182. https://doi.org/10.1016/j.chemosphere.2016.08.127
Mortan SH, Martin-Gonzalez L, Vicent T, Caminal G, Nijenhuis I, Adrian L, Marco-Urrea E (2017) Detoxification of 1,1,2-trichloroethane to ethene in a bioreactor co-culture of Dehalogenimonas and Dehalococcoides mccartyi strains. J Hazard Mater 331:218–225. https://doi.org/10.1016/j.jhazmat.2017.02.043
Mukerjee-Dhar G, Shimura M, Miyazawa D, Kimbara K, Hatta T (2005) bph genes of the thermophilic PCB degrader, Bacillus sp. JF8: characterization of the divergent ring-hydroxylating dioxygenase and hydrolase genes upstream of the Mn-dependent BphC. Microbiology 151:4139–4151. https://doi.org/10.1099/mic.0.28437-0
Murínová S, Dercová K, Dudášová H (2014) Degradation of polychlorinated biphenyls (PCBs) by four bacterial isolates obtained from the PCB-contaminated soil and PCB-contaminated sediment. Int Biodeterior Biodegrad 91:52–59. https://doi.org/10.1016/j.ibiod.2014.03.011
Nam IH, Chon CM, Jung KY, Kim JG (2014) Biodegradation of biphenyl and 2-chlorobiphenyl by a Pseudomonas sp. KM-04 isolated from PCBs-contaminated coal mine soil. Bull Environ Contam Toxicol 93:89–94. https://doi.org/10.1007/s00128-014-1286-6
Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J Hazard Mater 278:189–202. https://doi.org/10.1016/j.jhazmat.2014.05.051
Pathiraja G, Egodawatta P, Goonetilleke A, Te’o VSJ (2019) Solubilization and degradation of polychlorinated biphenyls (PCBs) by naturally occurring facultative anaerobic bacteria. Sci Total Environ 651:2197–2207. https://doi.org/10.1016/j.scitotenv.2018.10.127
Pathiraja G, Egodawatta P, Goonetilleke A, Te'o VSJ (2019) Effective degradation of polychlorinated biphenyls by a facultative anaerobic bacterial consortium using alternating anaerobic aerobic treatments. Sci Total Environ 659:507–514. https://doi.org/10.1016/j.scitotenv.2018.12.385
Payne RB, Fagervold SK, May HD, Sowers KR (2013) Remediation of polychlorinated biphenyl impacted sediment by concurrent bioaugmentation with anaerobic halorespiring and aerobic degrading bacteria. Environ Sci Technol 47:3807–3815. https://doi.org/10.1021/es304372t
Praveckova M, Brennerova MV, Holliger C, De Alencastro F, Rossi P (2016) Indirect evidence link PCB dehalogenation with Geobacteraceae in anaerobic sediment-free microcosms. Front Microbiol 7:933. https://doi.org/10.3389/fmicb.2016.00933
Qiao W, Luo F, Lomheim L, Mack EE, Ye S, Wu J, Edwards EA (2018) A Dehalogenimonas population respires 1,2,4-trichlorobenzene and dichlorobenzenes. Environ Sci Technol 52:13391–13398. https://doi.org/10.1021/acs.est.8b04239
Qiu L, Wang H, Wang X (2016) Isolation and characterization of a cold-resistant PCB209-degrading bacterial strain from river sediment and its application in bioremediation of contaminated soil. J Environ Sci Health A 51:204–212. https://doi.org/10.1080/10934529.2015.1094324
Rotaru AE, Woodard TL, Nevin KP, Lovley DR (2015) Link between capacity for current production and syntrophic growth in Geobacter species. Front Microbiol 6:744. https://doi.org/10.3389/fmicb.2015.00744
Salimizadeh M, Shirvani M, Shariatmadari H, Nikaeen M, Leili Mohebi Nozar S (2018) Coupling of bioaugmentation and phytoremediation to improve PCBs removal from a transformer oil-contaminated soil. Int J Phytoremediat 20:658–665. https://doi.org/10.1080/15226514.2017.1393388
Sandhu M, Jha P, Paul AT, Singh RP, Jha PN (2020) Evaluation of biphenyl- and polychlorinated-biphenyl (PCB) degrading Rhodococcus sp. MAPN-1 on growth of Morus alba by pot study. Int J Phytoremediat. https://doi.org/10.1080/15226514.2020.1784088
Sha’arani S, Hara H, Araie H, Suzuki I, Mohd Noor MJM, Akhir FNM, Othman N, Zakaria Z (2019) Whole gene transcriptomic analysis of PCB/biphenyl degrading Rhodococcus jostii RHA1. J Gen Appl Microbiol 65:173–179. https://doi.org/10.2323/jgam.2018.08.003
Sharma JK, Gautam RK, Nanekar SV, Weber R, Singh BK, Singh SK, Juwarkar AA (2017) Advances and perspective in bioremediation of polychlorinated biphenyl-contaminated soils. Environ Sci Pollut R 25:16355–16375. https://doi.org/10.1007/s11356-017-8995-4
Shuai J, Yu X, Zhang J, Xiong A, Xiong F (2016) Regional analysis of potential polychlorinated biphenyl degrading bacterial strains from China. Braz J Microbiol 47(3):536–541. https://doi.org/10.1016/j.bjm.2014.12.001
Steliga T, Wojtowicz K, Kapusta P, Brzeszcz J (2020) Assessment of biodegradation efficiency of polychlorinated biphenyls (PCBs) and petroleum hydrocarbons (TPH) in soil using three individual bacterial strains and their mixed culture. Molecules 25(3):709. https://doi.org/10.3390/molecules25030709
Su XM, Liu YD, Hashmi MZ, Ding LX, Shen CF (2015) Culture-dependent and culture-independent characterization of potentially functional biphenyl-degrading bacterial community in response to extracellular organic matter from Micrococcus luteus. Microb Biotechnol 8:569–578. https://doi.org/10.1111/1751-7915.12266
Suenaga H, Fujihara H, Kimura N, Hirose J, Watanabe T, Futagami T, Goto M, Shimodaira J, Furukawa K (2017) Insights into the genomic plasticity of Pseudomonas putida KF715, a strain with unique biphenyl-utilizing activity and genome instability properties. Environ Microbiol Rep 9:589–598. https://doi.org/10.1111/1758-2229.12561
Taguchi K, Motoyama M, Iida T, Kudo T (2007) Polychlorinated biphenyl/biphenyl degrading gene clusters in Rhodococcus sp. K37, HA99, and TA431 are different from well-known bph gene clusters of Rhodococci. Biosci Biotechnol Biochem 71:1136–1144. https://doi.org/10.1271/bbb.60551
Takeda H, Yamada A, Miyauchi K, Masai E, Fukuda M (2004) Characterization of transcriptional regulatory genes for biphenyl degradation in Rhodococcus sp. strain RHA1. J Bacteriol 186:2134–2146. https://doi.org/10.1128/jb.186.7.2134-2146.2004
Teng Y, Li X, Chen T, Zhang M, Wang X, Li Z, Luo Y (2016) Isolation of the PCB-degrading bacteria Mesorhizobium sp. ZY1 and its combined remediation with Astragalus sinicus L. for contaminated soil. Int J Phytoremediation 18:141–149. https://doi.org/10.1080/15226514.2015.1073667
Tomza-Marciniak A, Pilarczyk B, Witczak A, Rzad I, Pilarczyk R (2019) PCB residues in the tissues of sea ducks wintering on the south coast of the Baltic Sea, Poland. Environ Sci Pollut Res Int 26:11300–11313. https://doi.org/10.1007/s11356-019-04586-4
Voronina AO, Egorova DO, Korsakova ES, Plotnikova EG (2019) Diversity of the bphA1 genes in a microbial community from anthropogenically contaminated soil and isolation of new Pseudomonads degrading biphenyl/chlorinated biphenyls. Microbiology 88(4):433–443. https://doi.org/10.1134/S0026261719030172
Wagner DD, Hug LA, Hatt JK, Spitzmiller MR, Padilla-Crespo E, Ritalahti KM, Edwards EA, Konstantinidis KT, Loffler FE (2012) Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae. BMC Genomics 13:200. https://doi.org/10.1186/1471-2164-13-200
Wang H, Hu J, Xu K, Tang X, Xu X, Shen C (2018) Biodegradation and chemotaxis of polychlorinated biphenyls, biphenyls, and their metabolites by Rhodococcus spp. Biodegradation 29:1–10. https://doi.org/10.1007/s10532-017-9809-6
Wang S, Chng KR, Wilm A, Zhao S, Yang KL, Nagarajan N, He J (2014) Genomic characterization of three unique Dehalococcoides that respire on persistent polychlorinated biphenyls. P Natl Acad Sci USA 111:12103–12108. https://doi.org/10.1073/pnas.1404845111
Wang S, He J (2012) Two-step denaturing gradient gel electrophoresis (2S-DGGE), a gel-based strategy to capture full-length 16S rRNA gene sequences. Appl Microbiol Biotechnol 95:1305–1312. https://doi.org/10.1007/s00253-012-4251-5
Wang X, Teng Y, Luo Y, Dick RP (2016) Biodegradation of 3,3',4,4'-tetrachlorobiphenyl by Sinorhizobium meliloti NM. Bioresour Technol 201:261–268. https://doi.org/10.1016/j.biortech.2015.11.056
Warenik-Bany M, Maszewski S, Mikolajczyk S, Piskorska-Pliszczynska J (2019) Impact of environmental pollution on PCDD/F and PCB bioaccumulation in game animals. Environ Pollut 255:113159. https://doi.org/10.1016/j.envpol.2019.113159
Wójcik A, Perczyk P, Wydro P, Broniatowski M (2020) Dichlorobiphenyls and chlorinated benzoic acids-Emergent soil pollutants in model bacterial membranes. Langmuir monolayer and grazing incidence X-ray diffraction studies. J Mol Liq 307:112997. https://doi.org/10.1016/j.molliq.2020.112997
Wu Q, Milliken CE, Meier GP, Watts JE, Sowers KR, May HD (2002) Dechlorination of chlorobenzenes by a culture containing bacterium DF-1, a PCB dechlorinating microorganism. Environ Sci Technol 36:3290–3294. https://doi.org/10.1021/es0158612
Xing Z, Hu T, Xiang Y, Qi P, Huang X (2020) Degradation mechanism of 4-chlorobiphenyl by consortium of Pseudomonas sp. strain CB-3 and Comamonas sp. strain CD-2. Curr Microbiol 77:15–23. https://doi.org/10.1007/s00284-019-01791-9
Yang X, Liu X, Song L, Xie F, Zhang G, Qian S (2007) Characterization and functional analysis of a novel gene cluster involved in biphenyl degradation in Rhodococcus sp. strain R04. J Appl Microbiol 103:2214–2224. https://doi.org/10.1111/j.1365-2672.2007.03461.x
Yang Y, Higgins SA, Yan J, Simsir B, Chourey K, Iyer R, Hettich RL, Baldwin B, Ogles DM, Loffler FE (2017) Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes. ISME J 11:2767–2780. https://doi.org/10.1038/ismej.2017.127
Acknowledgements
This work was funded by the National Natural Science Fund of China (41671317), the Fundamental Research Funds for the Central Universities (KYYJ202002), and the Jiangsu Agriculture Science and Technology Innovation Fund (CX(18)1005).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Ethical statement
The authors declared that the work has been approved by Ethical Committee. And the work we submitted has not been published elsewhere, either completely, in part, or in another form. The manuscript has not been submitted to another journal and will not be published elsewhere.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Xiang, Y., Xing, Z., Liu, J. et al. Recent advances in the biodegradation of polychlorinated biphenyls. World J Microbiol Biotechnol 36, 145 (2020). https://doi.org/10.1007/s11274-020-02922-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-020-02922-2