Selective pressure of biphenyl/polychlorinated biphenyls on the formation of aerobic bacterial associations and their biodegradative potential

. 2021 Aug ; 66 (4) : 659-676. [epub] 20210508

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33966251

Grantová podpora
18-29-05016mk Russian Foundation of Basic Research

Odkazy

PubMed 33966251
DOI 10.1007/s12223-021-00873-1
PII: 10.1007/s12223-021-00873-1
Knihovny.cz E-zdroje

Unique bacterial associations were formed in the polluted soils from territory of the industrial factories Open Joint Stock Company "The Middle Volga Chemical Plant," Chapaevsk, Russia and Open Joint Stock Company "Lubricant Producing Plant," Perm, Russia. This study evaluates the influence of the biphenyl/polychlorinated biphenyls (PCB) on the formation of aerobic bacterial associations and their biodegradative potential. Enrichment cultivation of the soil samples from the territories of these industrial factories with PCB (commercial mixture Sovol) was lead for forming aerobic bacterial enrichment cultures showing a unique composition. The dominating in these bacterial cultures was the phylum Proteobacteria (Beta- and Gammaproteobacteria). Using biphenyl as a carbon source led to decrease of biodiversity in the final stable bacterial associations. Periodic cultivation experiments demonstrated that the association PN2-B has a high degradative potential among the six studied bacterial associations. PN2-B degraded 100% mono-chlorobiphenyls (94.5 mg/L), 86.2% di-chlorobiphenyls (22.3 mg/L), 50.9% Sovol, and 38.4% Delor 103 (13.8 mg/L). Qualitative analysis of metabolites showed that association performed transformation of chlorobenzoic acids (PCB degradation intermediates) into metabolites of citrate cycle. Twelve individual strain-destructors were isolated. The strains were found to degrade 17.7-100% PCB1, 36.2-100% PCB2, 18.8-100% PCB3 (94.5 mg/L), and 15.7-78.2% PCB8 (22.3 mg/L). The strains were shown to metabolize chlorobenzoic acids formed during degradation of chlorobiphenyls. A unique ability of strains Micrococcus sp. PNS1 and Stenotrophomonas sp. PNS6 to degrade ortho-, meta-, and para-monosubstituted chlorobenzoic acids was revealed. Our results suggest that PN2-B and individual bacterial strains will be perspective for cleaning of the environment from polychlorinated biphenyls.

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Agulló L, Pieper DH, Seeger M (2019) Genetics and biochemistry of biphenyl and PCB biodegradation. In: Rojo F. (eds) Aerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology. Springer, Cham, pp 595–622. https://doi.org/10.1007/978-3-319-50418-6_30

Arensdorf JJ, Focht DD (1995) A meta-cleavage pathway for 4-chlorobenzoate, an intermediate in the metabolism of 4-chlorobiphenyl by Pseudomonas cepacia P166. Appl Environ Microbiol 61:443–447 DOI

Atago Y, Shimodarira J, Araki N, Othman NB, Zakaria Z, Fukuda M, Futami J, Hara H (2016) Identification of novel extracellular protein for PCB/biphenyl metabolism in Rhodococcus jostii RHA1. Biosci Biotechnol Biochem 80:1012–1019. https://doi.org/10.1080/09168451.2015.1127134 PubMed DOI

Ausbel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (Eds) (1995) Short protocols in molecular biology, 3rd ed. New York: Wiley

Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300 DOI

Blanco-Moreno R, Sáez LP, Luque-Almagro VM, Roldán MD, Moreno-Vivián C (2017) Isolation of bacterial strains able to degrade biphenyl, diphenyl ether and the heat transfer fluid used in thermo-solar plants. New Biotechnol 35:35–41 DOI

Cervantes-González E, Guevara-Garcia MA, Garcia-Mena J, Ovando-Medina VM (2019) Microbial diversity assessment of polychlorinated biphenyl-contaminated soils and the biostimulation and bioaugmentation processes. Environ Monit Assess 191:118. https://doi.org/10.1007/s10661-019-7227-4 PubMed DOI

Chang Y-C, Takada K, Choi D, Toyama T, Sawada K, Kikuchi S (2013) Isolation of biphenyl and polychlorinated biphenyl-degrading bacteria and their degradation pathway. Appl Biochem Biotechnol 170:381–398. https://doi.org/10.1007/s12010-013-0191-5 PubMed DOI

Denef VJ, Klappenbach JA, Patrauchan MA, Florizone C, Rodrigues JLM, Tsoi TV, Verstraete W, Eltis LD, Tiedje JM (2006) Genetic and genomic insights into the role of benzoate-catabolic pathway redundancy in Burkholderia xenovorans LB400. Appl Environ Microbiol 72:585–595. https://doi.org/10.1128/AEM.72.1.585-595.2006 PubMed DOI PMC

Devi NL (2020) Persistent organic pollutants (POPs): environmental risks, toxicological effects, and bioremediation for environmental safety and challenges for future research. In: Saxena G., Bharagava R. (eds) Bioremediation of Industrial Waste for Environmental Safety. Springer, Singapore pp 53–76. https://doi.org/10.1007/978-981-13-1891-7_4

Egorova DO, Buzmakov SA (2020) Carcinogenic and teratogenic status of human population and polychlorinated biphenyls contaminations of soils and biota (European pied flycatcher) in a Perm (Western Ural, Russia). Environ Geochem Health 42:4299–4311. https://doi.org/10.1007/s10653-020-00615-1 PubMed DOI

Egorova DO, Korsakova ES, Demakov VA, Plotnikova EG (2013) Degradation of aromatic hydrocarbons by the Rhodococcus wratislaviensis KT112-7 isolated from waste products of a salt-mining plant. Appl Biochem Microbiol 49:244–255. https://doi.org/10.1134/S0003683813030071 DOI

Egorova DO, Pervova MG, Demakov VA, Plotnikova EG (2018) Specific features of chlorinated biphenyl decomposition by Rhodococcus wratislaviensis strain KT112-7 under high salt conditions. Appl Biochem Microbiol 54:252–261. https://doi.org/10.1134/S000368381803002X DOI

Egorova DO, Shumkova ES, Demakov VA, Plotnikova EG (2010) Degradation of chlorinated biphenyls and products of their bioconversion by Rhodococcus sp. B7a strain. Appl Biochem Microbiol 46:592–598. https://doi.org/10.1134/S0003683810060062 DOI

Fortin PD, Lo AT-F, Haro M-A, Kaschabek SR, Reineke W, Eltis LD (2005) Evolutionarily divergent extradiol dioxygenases possess higher specificities for polychlorinated biphenyl metabolites. J Bacteriol 187:415–421 DOI

Ge Y, Eltis LD (2003) Characterization of hybrid toluate and benzoate dioxigenases. J Bacteriol 185:5333–5341. https://doi.org/10.1128/JB.185.18.5333-5341.2003 PubMed DOI PMC

Gioia R, Akindele AJ, Adebusoye SA, Asante KA, Tanabe S, Buekens A, Sasco AJ (2014) Polychlorinated biphenyls (PCBs) in Africa: a review of environmental levels. Environ Sci Pollut Res 21:6278–6289. https://doi.org/10.1007/s11356-013-1739-1 DOI

Hatamian-Zarmi A, Shojaosadati SA, Vasheghani-Farahani E, Hosseinkhani S, Emamzadeh A (2009) Extensive biodegradation of highly chlorinated biphenyl and Aroclor 1242 by Pseudomonas aeruginosa TMU56 isolated from contaminated soils. Int Biodeter Biodegr 63:788–794. https://doi.org/10.1016/j.ibiod.2009.06.009 DOI

Hoostal MJ, Bouzat JL (2016) Spatial patterns of bphA gene diversity reveal local adaptation of microbial communities to PCB and PAH contaminants. Microbiol Ecol 72:559–570. https://doi.org/10.1007/s00248-016-0812-y DOI

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 PubMed DOI

Ilori MO, Robinson GK, Adebusoye SA (2008) Aerobic mineralization of 4,4’-dichlorobiphqnyl and 4-chlorobenzoic acid by a novel natural bacterial strain that grows poorly on benzoate and biphenyl. World J Microbiol Biotechnol 24:1259–1265. https://doi.org/10.1007/s11274-007-9597-y DOI

Isaac P, Sánchez LA, Bourguignon N, Cabral ME, Ferrero MA (2013) Indigenous PAH-degrading bacteria from oil-polluted sediments in Caleta Cordova, Patagonia Argentina. Int Biodeter Biodegr 82:207–214. https://doi.org/10.1016/j.ibiod.2013.03.009 DOI

ISO 18400–206:2018 (2018)Soil quality — sampling — Part 206: collection, handling and storage of soil under aerobic conditions for the assessment of microbiological processes, biomass and diversity in the laboratory. https://www.iso.org/obp/ui/#iso:std:iso:18400:-206:ed-1:v1:en

Jia Y, Wang J, Ren Ch, Naburira R, Khokhar I, Wang J, Fan S, Yan Y (2019) Identification and characterization of a meta-cleavage product hydrolase involved in biphenyl degradation from Arthrobacter sp. YC-RL1. Appl Microbiol Biotechnol 103:6825–6836. https://doi.org/10.1007/s00253-019-09956-z PubMed DOI

Kahlon RS (2016) Pseudomonas: genome and comparative genomics. In: Kahlon R. (eds) Pseudomonas: molecular and applied biology. Springer, Cham, pp 127–191. https://doi.org/10.1007/978-3-319-31198-2_4

Kim S, Picardal FW (2000) A novel bacterium that utilizes monochlorobiphenyls and 4-chlorobenzoate as a growth substrates. FEMS Microbiol Lett 185:225–229. https://doi.org/10.1111/j.1574-6968.2000.tb09066.x PubMed DOI

Kolar AB, Hršak D, Fingler S, Ćetković H, PetrićI KNU (2007) PCB-degrading potential of aerobic bacteria enriched from marine sediments. Int Biodeter Biodegr 60:16–24. https://doi.org/10.1016/j.ibiod.2006.11.004 DOI

Liu Ch, Wei BK, Bao JS, Wang Y, Hu JCh, Tang YE, Chen T, Jin J (2020) Polychlorinated biphenyls in the soil-crop-atmosphere system in e-waste dismantling areas in Taizhou: concentrations, congener profiles, uptake, and translocation. Environ Pollut 257:113622 DOI

Liz JAZE, Jan-Roblero J, de la Serna JZD, de León AVP, Hernández-Rodriguez C (2009) Degradation of polychlorinated biphenyl (PCB) by a consortium obtained from a contaminated soil composed of Brevibacterium, Pandoraea and Ochrobactrum. World J Microbiol Biotechnol 25:165–170. https://doi.org/10.1007/s11274-008-9875-3 DOI

Malina N, Mazlova EA, Kulikova O (2020) Markers of polychlorinated biphenyl (PCB) degradation in highly contaminated soil of Central Russia. Environ Sci Pollut Res 27:36587–36595. https://doi.org/10.1007/s11356-020-09712-1 DOI

Murinová S, Dercová K (2014) Potential use of newly isolated bacterial strain Ochrobactrum anthropi in bioremediation of polychlorinated biphenyls. Water Air Soil Pollut 225:1980. https://doi.org/10.1007/s11270-014-1980-3 DOI

Murinová 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 Biodeter Biodegr 91:52–59. https://doi.org/10.1016/j.ibiod.2014.03.011 DOI

Nam I-H, Chon C-M, Jung K-Y, Kim J-G (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 PubMed DOI

Nazarov AV, Egorova DO, Makarenko AA, Demakov VA, Plotnikova EG (2016) Ecological-microbiological assessment of polychlorinated biphenyl-contaminated grounds. Hum Ecol 3:3–8. https://doi.org/10.33396/1728-0869-2016-3-3-8

Papale M, Giannarelli S, Francesconi S, Di Marco G, Mikkonen A, Conte A, Rizzo C, De Domenico E, Michaud L, Giudice AL (2017) Enrichment, isolation and biodegradation potential of psychrotolerant polychlorinated-biphenyl degrading bacteria from the Kongsfjorden (Svalbard Islands, High Arctic Norway). Mar Pollut Bull 114:849–859. https://doi.org/10.1016/j.marpolbul.2016.11.011 PubMed DOI

Parales RE, Resnick SM (2006) Aromatic ring hydroxylating dioxygenases. In: Ramos JL., Levesque R.C. (eds) Pseudomonas. Springer, Boston, MA pp 287–340. https://doi.org/10.1007/0-387-28881-3_9

Petrić I, Hršak D, Fingler S, Udiković-Kolić N, Bru D, Martin-Laurent F (2011) Insight in the PCB-degrading functional community in long-term contaminated soil under bioremediation. J Soils Sediments 11:290–300. https://doi.org/10.1007/s11368-010-0299-y DOI

Plotnikova EG, Egorova DO, Shumkova ES, Solyanikova IP, Golovleva LA (2012) Degradation of 4-chlorobiphenyl and 4-chlorobenzoic acid by the strain Rhodococcus ruber P25. Microbiology 81:143–153. https://doi.org/10.1134/S0026261712020117 DOI

Ponce BL, Latorre VK, González M, Seeger M (2011) Antioxidant compounds improved PCB-degradation by Burkholderia xenovorans strain LB400. Enzime Microb Tech 49:509–516. https://doi.org/10.1016/j.enzmictec.2011.04.021 DOI

Providenti MA, Wyndham RC (2001) Identification and functional characterization of CbaR, a MarR-like modulator of the cbaABC-encoded chlorobenzoate catabolism pathway. Appl Environ Microbiol 67:3530–3541. https://doi.org/10.1128/AEM.67.8.3530-3541.2001 PubMed DOI PMC

Reddy AVB, Moniruzzaman M, Aminabhavi TM (2019) Polychlorinated biphenyls (PCBs) in the environment: recent updates on sampling, pretreatment, cleanup technologies and their analysis. Chem Eng J 358:11860–21207. https://doi.org/10.1016/j.cej.2018.09.205 DOI

Rybkina DO, Plotnikova EG, Demakov VA, Dorofeeva LV, Mironenko YuL (2003) A new aerobic gram-positive bacterium with a unique ability to degrade ortho- and para-chlorinated biphenyls. Microbiology 72:672–677. https://doi.org/10.1023/B:MICI.0000008367.24540.6c DOI

Salam AB, Idris H (2019) Consequences of crude oil contamination on the structure and function of autochthonous microbial community of a tropical agricultural soil. Environ Sustain 2:167–187. https://doi.org/10.1007/s42398-019-00058-0 DOI

Seah SYK, Labbe G, Kaschebek SR, Reifenrath F, Reineke W, Eltis LD (2001) Comparative specificities of two evolutionarily divergent hydrolases involved in microbial degradation of polychlorinated biphenyls. J Bacteriol 183:1511–1516. https://doi.org/10.1128/JB.183.5.1511-1516.2001 PubMed DOI PMC

Seah SYK, Labbe G, Nerdinger S, Johnson MR, Snieckus V, Eltis LD (2000) Identification of a serine hydrolase as a key determinant in the microbial degradation of polychlorinated biphenyls. J Biol Chem 275:15701–15708. https://doi.org/10.1074/jbc.275.21.15701 PubMed DOI

Shah V, Zakrzewski M, Wibberg D, Eikmeyer F, Schlüter A, Madamwar D (2013) Taxanomic profiling and metagenome analysis of a microbial community from a habitat contaminated with industrial discharges. Microbiol Ecol 66:533–550. https://doi.org/10.1007/s00248-013-0253-9 DOI

Su X, Li S, Cai J, Xiao Y, Tao L, Hashmi MZ, Lin H, Chen J, Mei R, Sun F (2019) Aerobic degradation of 3,3’,4,4’-tetrachlorobiphenyl by a resuscitated strain Castellaniella sp. SPC4: kinetics model and pathway. Sci Total Environ 688:917–925. https://doi.org/10.1016/scitotenv.2019.06.364 PubMed DOI

Su X, Shen H, Yao X, Ding L, Yu Ch, Shen Ch (2013) A novel approach to stimulate the biphenyl-degrading potential of bacterial community from PCBs-contaminated soil of e-waste recycling sites. Bioresource Technol 146:27–34 DOI

Su X, Zhang Q, Hu J, Hashmi Z, Ding L, Shen Ch (2015) Enhanced degradation of biphenyl from PCB-contaminated sediments: the impact of extracellular organic matter from Micrococcus luteus. Appl Microbiol Biotechnol 99:1989–2000. https://doi.org/10.1007/s00253-014-6108-6 PubMed DOI

Tiirola MA, Busse HJ, Kampfer P, Mannisto MK (2005) Novosphingobium lentum sp. Nov., a psychrotolerant bacterium from a polychlorophenol bioremediation process. Int J Syst Evol Microbiol 55:583–588. https://doi.org/10.1099/ijs.0.63386-0 PubMed DOI

Uhlik O, Musilova L, Ridl J, Hroudova M, Vlcek C, Koubek J, Holeckova M, Mackova M, Macek T (2013) Plant secondary metabolite-induced shifts in bacterial community structure and degradative ability in contaminated soil. Appl Microbiol Biotechnol 97:9245–9256. https://doi.org/10.1007/s00253-012-4627-6 PubMed DOI

Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Meth Cell Mol Biol 5:25–40

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 88:433–443. https://doi.org/10.1134/S0026261719030172 DOI

Wu M, Chen L, Tian Y, Ding Y, Dick WA (2013) Degradation of polycyclic aromatic hydrocarbons by microbial consortia enriched from three soils using two different culture media. Environ Pollut 178:152–158. https://doi.org/10.1016/j.envpol.2013.03.004 PubMed DOI

Zaitsev GM, Tsoi TV, Grishenkov VG, Plotnikova EG, Boroni AM (1991) Genetic control of degradation of chlorinated benzoic acids in Arthrobacter globiformis, Corynebacterium sepedonicum and Pseudomonas cepacia strains. FEMS Microbiol Lett 81:171–176 DOI

Zentero-Rojas A, Martínez-Romero E, Castañeda-Valbuena D, Ivette Rincón-Molina C, Ruíz-Valdiviezo VM, Meza-Gordillo R, Villalobos-Maldonado JJ, Vences-Guzmán MÁ, Rincón-Rosales R (2020) Structure and diversity of native bacterial communities in soils contaminated with polychlorinated biphenyls. AMB Expr 10:124. https://doi.org/10.1186/s13568-020-01058-8 DOI

Zhang Y, Deng ChP, Shen B, Yang J-S, Wang ET, Yuan HL (2016) Syntrophic interactions within a butane-oxidixing bacterial consortium isolated from Puguang gas field in China. Microbiol Ecol 72:538–548. https://doi.org/10.1007/s00248-016-0799-4 DOI

Zhang W, Wang H, Zhang R, Yu X-Z, Qian P-Y, Wong MH (2010) Bacterial communities in PAH contaminated soils at an electronic-waste processing center in China. Ecotoxicology 19:96–104. https://doi.org/10.1007/s10646-009-0393-3 PubMed DOI

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