Characterization of a highly enriched microbial consortium reductively dechlorinating 2,3-dichlorophenol and 2,4,6-trichlorophenol and the corresponding cprA genes from river sediment

• Autorzy: El-Sayed W.S.
• Języki publikacji: EN

Abstrakty

EN

Anaerobic reductive dechlorination of 2,3-dichlorophenol (2,3DCP) and 2,4,6-trichlorophenol (2,4,6TCP) was investigated in microcosms from River Nile sediment. A stable sediment-free anaerobic microbial consortium reductively dechlorinating 2,3DCP and 2,4,6TCP was established. Defined sediment-free cultures showing stable dechlorination were restricted to ortho chlorine when enriched with hydrogen as the electron donor, acetate as the carbon source, and either 2,3-DCP or 2,4,6-TCP as electron acceptors. When acetate, formate, or pyruvate were used as electron donors, dechlorination activity was lost. Only lactate can replace dihydrogen as an electron donor. However, the dechlorination potential was decreased after successive transfers. To reveal chlororespiring species, the microbial community structure of chlorophenol-reductive dechlorinating enrichment cultures was analyzed by PCR-denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments. Eight dominant bacteria were detected in the dechlorinating microcosms including members of the genera Citrobacter, Geobacter, Pseudomonas, Desulfitobacterium, Desulfovibrio and Clostridium. Highly enriched dechlorinating cultures were dominated by four bacterial species belonging to the genera Pseudomonas, Desulfitobacterium, and Clostridium. Desulfitobacterium represented the major fraction in DGGE profiles indicating its importance in dechlorination activity, which was further confirmed by its absence resulting in complete loss of dechlorination. Reductive dechlorination was confirmed by the stoichiometric dechlorination of 2,3DCP and 2,4,6TCP to metabolites with less chloride groups and by the detection of chlorophenol RD cprA gene fragments in dechlorinating cultures. PCR amplified cprA gene fragments were cloned and sequenced and found to cluster with the cprA/pceA type genes of Dehalobacter restrictus.

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2016
• Tom: 65
• Numer: 3
• Opis fizyczny: p.341-352,fig.,ref.

Twórcy

autor

El-Sayed W.S.

• Biology Department, Faculty of Science, Taibah University, Almadinah Almunawarah, KSA, Egypt
• Microbiology Department, Faculty of Science, Ain Shams University, Cairo, Egypt

Bibliografia

• Alder A., C.M.M. Häggblom, S.R. Oppenheimer and L.Y. Young. 1993. Reductive dechlorination of polychlorinated biphenyls in anaerobic sediments. Environ. Sci. Technol. 27: 530–538.
• Altschul S.F., T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang,W. Miller and D.J. Lipman. 1997. Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acid Res. 25: 3389–3402.
• Bouchard B., R. Beaudet, R. Villemur, G. McSween, F. Lepine and J.G. Bisaillon. 1996. Isolation and characterization of Desulfitobacterium frappieri sp. nov., an anaerobic bacterium which reductively dechlorinates pentachlorophenol to 3-chlorophenol. Int. J. Syst. Bacteriol. 46: 1010–1015.
• Breitenstein A., A. Saano, M. Salkinoja-Salonen, J.R. Andreesen and U. Lechner. 2001. Analysis of a 2,4,6-trichlorophenol-dehalogenating enrichment culture and isolation of the dehalogenating member Desulfitobacterium frappieri strain TCP-A. Arch. Microbiol. 175: 133–142.
• Brisson V.L., K.A. West, P.K.H. Lee, S.G. Tringe, E.L. Brodie and L. Alvarez-Cohen. 2012. Metagenomic analysis of a stable trichloroethene-degrading microbial community. ISME J. 6: 1702–1714.
• Christiansen N. and B.K. Ahring. 1996. Desulfitobacterium hafniense sp. nov., an anaerobic, reductively dechlorinating bacterium. Int. J. Syst. Bacteriol. 46: 442–448.
• Christiansen N., B.K. Ahring, G. Wohlfarth and G. Diekert. 1998. Purification and characterization of the 3-chloro-4-hydroxy-phenylacetate reductive dehalogenase of Desulfitobacterium hafniense. FEBS Lett. 436: 159–162.
• Chrzanowski L., L.Y. Wick, R. Meulenkamp, M. Kaestner and H.J. Heipieper. 2009. Rhamnolipid biosurfactants decrease the toxicity of chlorinated phenols to Pseudomonas putida DOT-T1E. Lett. App. Microbiol. 48: 756–762.
• Chrzanowski L., M. Owsianiak, A. Szulc, R. Marecik, A.P. Cyplik,A.K.O Schmidt, J. Staniewski, P. Lisiecki, F. Ciesielczyk, T. Jesionowski and others. 2011. Interactions between rhamnolipid biosurfactants and toxic chlorinated phenols enhance biodegradation of a model hydrocarbon-rich effluent. International Biodeterioration and Biodegradation 65:605–611.
• Cole J.R., A.L. Cascarelli, W.W. Mohn and J.M. Tiedje. 1994. Isolation and characterization of a novel bacterium growing via reductive dehalogenation of 2-chlorophenol. Appl. Environ. Microbiol. 60: 3536–3542.
• Cupples A.M., R.A. Sanford and G.K. Sims. 2005. Dehalogenation of the herbicides bromoxynil (3,5-dibromo-4-hydroxybenzonitrile) and ioxynil (3,5-diiodino-4-hydroxybenzonitrile) by Desulfitobacterium chlororespirans. Appl. Environ. Microbiol. 71: 3741–3746.
• Deweerd K.A., L. Mandelco, R.S. Tanner, C.R. Woese andJ.M. Suflita. 1990. Desulfomonile tiedjei gen. nov. and sp. nov., a novel anaerobic, dehalogenating, sulfate-reducing bacterium. Arch. Microbiol. 154: 23–30.
• Drzyzga O., J. Gerritse, J.A. Dijk, H. Elissen and J.C. Gottschal. 2001. Coexistence of a sulphate-reducing Desulfovibrio species and the dehalorespiring Desulfitobacterium frappieri TCE1 in defined chemostat cultures grown with various combinations of sulfate and tetrachloroethene. Environ. Microbiol. 3(2): 92–99.
• Duhamel M. and E.A. Edwards. 2007. Growth and yields of dechlorinators, acetogens, and methanogens during reductive dechlorination of chlorinated ethenes and dihaloelimination of 1,2-dichloro-ethane. Environ. Sci. Technol. 41: 2303–2310.
• El Fantroussi S., H. Naveau and S.N. Agathos. 1998. Anaerobic dechlorinating bacteria. Biotechnol. Prog. 14: 167–188.
• Fagervold S.K., J.E.M. Watts, H.D. May and K.R. Sowers. 2005. Sequential reductive dechlorination of meta-chlorinated polychlorinated biphenyl congeners in sediment microcosms by two different Chloroflexi phylotypes. Appl. Environ. Microbiol. 71(12): 8085–8090.
• Fennell D.E., V. Nijenhuis, S.F. Wilson, S.H. Zinder andM.M. Häggblom. 2004. Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ. Sci. Technol. 38: 2075–2081.
• Fung J.M., B.P. Weisenstein, E.E. Mack, J.E. Vidumsky, T.A. Ei and S.H. Zinder. 2009. Reductive dehalogenation of dichlorobenzenes and monochlorobenzene to benzene in microcosms. Environ. Sci. Technol. 43: 2302–2307.
• Gauthier A., R. Beaudet, F. Le´pine, P. Juteau and R. Villemur. 2006. Occurrence and expression of crdA and cprA5 encoding chloroaromatic reductive dehalogenases in Desulfitobacterium strains. Can. J. Microbiol. 52(1): 47–55.
• Gelsomino A., C. Keijzer-Wolters, G. Cacco and J.D. van Elsas. 1999. Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. J. Microbiol. Methods 38: 1–15.
• Gerritse J., V. Renard, P.T.M. Gomes, P.A. Lawson, M.D. Collins and J.C. Gottschal. 1996. Desulfitobacterium sp. strain PCE1, an anaerobic bacterium that can grow by reductive dechlorination of tetrachloroethene or ortho-chlorinated phenols. Arch. Microbiol. 165(2): 132–40.
• Gerritse J., O. Drzyzga, G. Kloetstra, M. Keijmel, L.P. Wiersum, R. Hutson, M.D. Collins and J.C. Gottschal. 1999. Influence of different electron donors and acceptors on dehalorespiration of tetrachloroethene by Desulfitobacterium frappieri TCE1. Appl. Environ. Microbiol. 65(12): 5212–5221.
• Häggblom M.M. 1992. Microbial breakdown of halogenated aromatic pesticides and related compounds. FEMS Microbiol. Rev. 103: 29–71.
• Häggblom M.M. and I.G. Bossert (eds). 2003. Dehalogenation, microbial processes and environmental applications. Kluwer Academic Publisher Group, Norwell, MA.
• Holliger C., G. Wohlfarth and G. Diekert. 1998. Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol. Rev. 22: 383–398.
• Holliger C., C. Regeard and G. Diekert. 2003. Dehalogenation by anaerobic bacteria, pp. 115–157. In: Häggblom M.M. and I.D. Bossert(eds). Dehalogenation, Microbial Processes and Environmental Applications. Kluwer Academic Publisher Group, Norwell, MA.
• Hug L.A. 2012. Ph.D. Thesis. A metagenome-based examination of dechlorinating enrichment cultures: Dehalococcoides and the role of the non-dechlorinating microorganisms, pp. 1–264. Cell and Systems Biology, University of Toronto, Canada.
• Hug L.A. and E.A. Edwards. 2013. Diversity of reductive dehalogenase genes from environmental samples and enrichment cultures identified with degenerate primer PCR screens. Front. Microbiol. 49(341): 1–16.
• Hug L.A., F. Maphosa, D. Leys, F.E. Löffler, H. Smidt, E.A. Edwardsand L. Adrian. 2013. Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Phil. Trans R. Soc. B. 368: 20120322.
• Itoh K., Y. Mihara, N. Tanimoto, T. Shimada and K. Suyama. 2010. Reductive dechlorination of chlorophenols in estuarine sediments of Lake Shinji and Lake Nakaumi. J. Environ. Sci. Health B. 45(5): 399–407.
• Karn S.K., S.K. Chakrabarti and M.S. Reddy. 2011. Degradation of pentachlorophenol by Kocuria sp. CL2 isolated from secondary sludge of pulp and paper mill. Biodegradation 22: 63–69.
• Kjellerup B.V., C. Naff, S.J. Edwards, U. Ghosh, J.E. Baker and K.R. Sowers. 2014. Effects of activated carbon on reductive dechlorination of PCBs by organohalide respiring bacteria indigenous to sediments. Water Res. 52: 1–10.
• Kumar S., K. Tamura and M. Nei. 2004. MEGA3: An integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 5: 150–163.
• Kuokkaa S., A.L. Rantalainena, M. Romantschuka and M.M. Häggblom. 2014. Effect of temperature on the reductive dechlorinationof 1,2,3,4-tetrachlorodibenzofuran in anaerobicPCDD/F-contaminated sediments. J. Haz. Mat. 274: 72–78.
• Lake J.L., R.J. Pruell and F.A. Osterman. 1992. An examination of dechlorination processes and pathways in New Bedford Harbor sediments. Mar. Environ. Res. 33: 31–47.
• Leys D., L. Adrian and H. Smidt. 2013. Organohalide respiration: microbes breathing chlorinated molecules. Phil. Trans R. Soc. B. 368: 20120316.
• Li Z., Y. Inoue, D. Suzuki, L. Ye and A. Katayama. 2013. Long-term anaerobic mineralization of pentachlorophenol in a continuous-flow system using only lactate as an external nutrient. Environ. Sci. Technol. 47: 1534–1541.
• Löffler F.E., R.A. Sanford and J.M. Tiedje. 1996. Initial characterization of a reductive dehalogenase from Desulfitobacterium chlororespirans Co23. Appl. Environ. Microbiol. 62: 3809–3813.
• Löffler F.E., J.R. Cole, K.M. Ritalahti and J.M. Tiedje. 2003. Diversity of dechlorinating bacteria. Dehalogenation, pp. 53–87. In: Häggblom M.M. and I.D. Bossert (eds). Microbial processes and environmental applications. Kluwer Academic Publisher Group, Norwell, MA.
• Luijten M., W. Roelofsen, A.A.M. Langenhoff, G. Schraa and A.J.M. Stams. 2004. Hydrogen threshold concentrations in pure cultures of halorespiring bacteria and at a site polluted with chlorinated ethenes. Environ. Microbiol. 6: 646–650.
• Madsen T. and D. Licht. 1992. Isolation and characterization of an anaerobic chlorophenol-transforming bacterium. Appl. Environ. Microbiol. 58:2874–2878.
• Maphosa F., M.W.J. van Passel, W.M. de Vos and H. Smidt. 2012. Metagenome analysis reveals yet unexplored reductive dechlorinating potential of Dehalobacter sp. E1 growing in co-culture with Sedimentibacter sp. Environ. Microbiol. Rep. 4: 604–616.
• Masunaga S., S. Susarla, J.L. Gundersen and Y. Yonezawa. 1996. Pathways and rate of chlorophenol transformation in anaerobic estuarine sediment. Environ. Sci. Technol. 30: 1253–1260.
• Maymo-Gatell X., Y.T. Chien, J.M. Gossett and S.H. Zinder. 1997. Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276: 1568–1571.
• Mazur C.S. and W.J. Jones. 2001. Hydrogen concentrations in sulfate-reducing estuarine sediments during PCE dehalogenation. Environ. Sci. Technol. 35: 4783–4788.
• Mazur C.S., W.J. Jones and C.T. Stevens. 2003. H2 consumption during the microbial reductive dehalogenation of chlorinated phenols and tetrachloroethene. Biodegradation 14:(4) 285–295.
• McAllister K.A., H. Lee and J.T. Trevors. 1996. Microbial degradation of pentachlorophenol. Biodegradation 7: 1–40.
• Muyzer G., E. de Waal and A. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695–700.
• Rowe A.R., B.J. Lazar, R.M. Morris and R.E. Richardson. 2008. Characterization of the community structure of a dechlorinating mixed culture and comparisons of gene expression in planktonic and biofloc-associated Dehalococcoides and Methanospirillum species. Appl. Environ. Microbiol. 74: 6709–6719.
• Saitou N. and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
• Sanford R.A., J.R. Cole, F.E. Löffler and J.M. Tiedje. 1996. Characterization of Desulfitobacterium chlororespirans sp. nov., which grows by coupling the oxidation of lactate to the reductive dechlorination of 3-chloro-4-hydroxybenzoate. Appl. Environ. Microbiol. 62: 3800–3808.
• Sanford R.A., J.R. Cole and J.M. Tiedje. 2002. Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl. Environ. Microbiol. 68: 893–900.
• Sanger F., S. Nicklen and A.R. Coulson. 1977. DNA sequencing with chain-termination inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.
• Smidt H., M. van Leest, J. van der Oost and W.M. de Vos. 2000. Transcriptional regulation of the cpr gene cluster in ortho-chlorophenol-respiring Desulfitobacterium dehalogenans. J. Bacteriol. 182(20): 5683–5691.
• Smidt H. and W.M. de Vos. 2004. Anaerobic microbial dehalogenation. Annu. Rev. Microbiol. 58: 43–73.
• Sun B., J.R. Cole, R.A. Sanford and J.M. Tiedje. 2000. Isolation and characterization of Desulfovibrio dechloracetivorans sp. nov., a marine dechlorinating bacterium growing by coupling the oxidation of acetate to the reductive dechlorination of 2 chlorophenol. Appl. Environ. Microbiol. 66(6): 2408–2413.
• Takeuchi R., Y. Suwa, T. Yamagishi and Y. Yonezawa. 2000. Anaerobic transformation of chlorophenols in methanogenic sludge unexposed to chlorophenols. Chemosphere 41:1457–1462.
• Thibodeau J., A. Gauthier, M. Duguay, R. Villemur, F. Le’pine,P. Juteau and R. Beaudet. 2004. Purification, cloning, and sequencing of a 3,5-dichlorophenol reductive dehalogenase from Desulfitobacterium frappieri PCP-1. Appl. Environ. Microbiol. 70: 4532–4537.
• Thomas S.H., R.D. Wagner, A.K. Arakaki, J. Skolnick, J.R. Kirby, L.J. Shimkets, R.A. Sanford and F.E. Löffler. 2008. The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria. PLoS ONE 3(5): e2103.
• Thompson D., J. Gibson, F. Plewinak, F. Jeanmougin and G. Higgins. 1997. The Clastal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc. Acid Res. 25: 4867–4887.
• Utkin I., C. Woese and J. Wiegel. 1994. Isolation and characteriza-tion of Desulfitobacterium dehalogenans gen. nov., sp. nov., an anaerobic bacterium which reductively dechlorinates chlorophenolic compounds. Int. J. Syst. Bacteriol. 44: 612–619.
• van de Pas B.A., H. Smidt, W.R. Hagen, J. van der Oost, G. Schraa, A.J. Stams and W.M. de Vos. 1999. Purification and molecular characterization of ortho-chlorophenol reductive dehalogenase, a key enzyme of halorespiration in Desulfitobacterium dehalogenans. J. Biol. Chem. 274: 20287–20292.
• Vandermeeren P., S. Herrmann, D. Cichocka, P. Busschaert, B. Lievens, H.H. Richnow and D. Springael. 2014. Diversity of dechlorination pathways and organohalide respiring bacteria in chlorobenzene dechlorinating enrichment cultures originating from river sludge. Biodegradation. 25(5): 757–776.
• von Wintzingerode F., C. Schlötelburg, R. Hauck, W. Hegemann and U.B. Göbel. 2001. Development of primers for amplifying genes encoding CprA- and PceA-like reductive dehalogenases in anaerobic microbial consortia, dechlorinating trichlorobenzene and 1,2-dichloropropane. FEMS Microbiol. Ecol. 35: 189–196.
• Villemur R., M. Saucier, A. Gauthier and R. Beaudet. 2002. Occurrence of several genes encoding putative reductive dehalogenases in Desulfitobacterium hafniense/frappieri and Dehalococcoides ethenogenes. Can. J. Microbiol. 48(8): 697–706.
• Villemur R., M. Lanthier, R. Beaudet and F. L´epine. 2006. The Desulfitobacterium genus FEMS Microbiol. Rev. 30:706–733.
• Villemur R. 2013. The pentachlorophenol-dehalogenating Desulfitobacterium hafniense strain PCP-1. Philos. Trans R. Soc. B. 368(1616): 20120319.
• Wagner D.D., L.A. Hug, J.K. Hatt, M.A. Spitzmiller, E. Padilla-Crespo, K.M. Ritalahti, E.A. Edward, K.T. Konstantinidis and F.E. Löffler. 2012. Genomic determinants of organohalide-respiration in Geobacter lovleyi, an unusual member of the Geobacteraceae. BMC Genomics 13(200): 1–17.
• Wang S., W. Zhang, K.L. Yang and J. He. 2014. Isolation and characterization of a novel Dehalobacter species strain TCP1 that reductively dechlorinates 2,4,6-trichlorophenol. Biodegradation. 25(2): 313–323.
• WHO. 1998. Guidelines for Drinking-Water Quality, 2nd eds. Addendum to Vol. 1, Recommendations, pp. 21–22. World Health Organization, Geneva.
• WHO. 1989. Chlorophenols other than pentachlorophenol. World Health Organization, Geneva.
• Wiegel J., X.M. Zhang and Q.Z. Wu. 1999. Anaerobic dehalogenation of hydroxylated polychlorinated biphenyls by Desulfitobacterium dehalogenans. Appl. Environ. Microbiol. 65: 2217–2221.
• Wu Q.Z., K.R. Sowers and H.D. May. 1998. Microbial reductive dechlorination of Aroclor 1260 in anaerobic slurries of estuarine sediments. Appl. Environ. Microbiol. 64: 1052–1058.
• Zanaroli G., A. Balloi, A. Negroni, D. Daffonchio, L.Y. Young and F. Fava. 2010. Characterization of the microbial community from the marine sediment of the Venice lagoon capable of reductive dechlorination of coplanar polychlorinated biphenyls (PCBs). J. Haz. Mat. 178: 417–426.

Identyfikatory

DOI

10.5604/17331331.1215613