Indirect Evidence Link PCB Dehalogenation with Geobacteraceae in Anaerobic Sediment-Free Microcosms

. 2016 ; 7 () : 933. [epub] 20160616

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27379063

Although polychlorinated biphenyls (PCBs) production was brought to a halt 30 years ago, recalcitrance to degradation makes them a major environmental pollutant at a global scale. Previous studies confirmed that organohalide-respiring bacteria (OHRB) were capable of utilizing chlorinated congeners as electron acceptor. OHRB belonging to the Phyla Chloroflexi and Firmicutes are nowadays considered as the main PCB-dechlorinating organisms. In this study, we aimed at exploring the involvement of other taxa in PCB dechlorination using sediment-free microcosms (SFMs) and the Delor PCB mixture. High rates of congener dehalogenation (up to 96%) were attained in long-term incubations of up to 692 days. Bacterial communities were dominated by Chloroflexi, Proteobacteria, and Firmicutes, among strictly simplified community structures composed of 12 major phyla only. In a first batch of SFMs, Dehalococcoides mccartyi closely affiliated with strains CG4 and CBDB1 was considered as the main actor associated with congener dehalogenation. Addition of 2-bromoethanesulfonate (BES), a known inhibitor of methanogenic activity in a second batch of SFMs had an adverse effect on the abundance of Dehalococcoides sp. Only two sequences affiliated to this Genus could be detected in two (out of six) BES-treated SFMs, contributing to a mere 0.04% of the communities. BES-treated SFMs showed very different community structures, especially in the contributions of organisms involved in fermentation and syntrophic activities. Indirect evidence provided by both statistical and phylogenetic analysis validated the implication of a new cluster of actors, distantly affiliated with the Family Geobacteraceae (Phylum δ-Proteobacteria), in the dehalogenation of low chlorinated PCB congeners. Members of this Family are known already for their dehalogenation capacity of chlorinated solvents. As a result, the present study widens the knowledge for the phylogenetic reservoir of indigenous PCB dechlorinating taxa.

Zobrazit více v PubMed

Adrian L., Dudková V., Demnerová K., Bedard D. L. (2009). “ PubMed DOI PMC

Becker J. G., Berardesco G., Rittmann B. E., Stahl D. A. (2005). The role of syntrophic associations in sustaining anaerobic mineralization of chlorinated organic compounds. Environ. Health Perspect. 113, 310–316. 10.1289/ehp.6933 PubMed DOI PMC

Bedard D. L. (2008). A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls - from sediment to defined medium. Annu. Rev. Microbiol. 62, 253–270. 10.1146/annurev.micro.62.081307.162733 PubMed DOI

Bedard D. L. (2014). PCB dechlorinases revealed at last. Proc. Natl. Acad. Sci. U.S.A. 111, 11919–11920. 10.1073/pnas.1412286111 PubMed DOI PMC

Bedard D. L., Bailey J. J., Reiss B. L., Jerzak G. V. S. (2006). Development and characterization of stable sediment-free anaerobic bacterial enrichment cultures that dechlorinate Aroclor 1260. Appl. Env. Microbiol. 72, 2460–2470. 10.1128/AEM.72.4.2460-2470.2006 PubMed DOI PMC

Bedard D. L., Ritalahti K. M., Löffler F. E. (2007). The PubMed DOI PMC

Borrel G., O'Toole P. W., Harris H. M. B., Peyret P., Brugère J.-F., Gribaldo S. (2013). Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol. Evol. 5, 1769–1780. 10.1093/gbe/evt128 PubMed DOI PMC

Boyd J. M., Ellsworth A., Ensign S. A. (2006). Characterization of 2-bromoethanesulfonate as a selective inhibitor of the coenzyme m-dependent pathway and enzymes of bacterial aliphatic epoxide metabolism. J. Bacteriol. 188, 8062–8069. 10.1128/JB.00947-06 PubMed DOI PMC

Brown J. F., Wagner R. E., Bedard D. L. (1988). Response: PCB dechlorination in Hudson River sediment. Science 240, 1675–1676. 10.1126/science.240.4859.1675 PubMed DOI

Cai Y., Sun Y. (2011). ESPRIT-Tree: hierarchical clustering analysis of millions of 16S rRNA pyrosequences in quasilinear computational time. Nucleic Acids Res. 39, e95. 10.1093/nar/gkr349 PubMed DOI PMC

Cutter L., Sowers K. R., May H. D. (1998). Microbial dechlorination of 2,3,5,6-tetrachlorobiphenyl under anaerobic conditions in the absence of soil or sediment. Appl. Environ. Microbiol. 64, 2966–2969. PubMed PMC

Cutter L. A., Watts J. E., Sowers K. R., May H. D. (2001). Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl. Environ. Microbiol. 3, 699–709. 10.1046/j.1462-2920.2001.00246.x PubMed DOI

Dercová K., Čičmanová J., Lovecká P., Demnerová K., Macková M., Hucko P., et al. (2008). Isolation and identification of PCB-degrading microorganisms from contaminated sediments. Int. Biodeterior. Biodegrad. 62, 219–225. 10.1016/j.ibiod.2008.01.016 DOI

Diaby N., Dold B., Rohrbach E., Holliger C., Rossi P. (2015). Temporal evolution of bacterial communities associated with the PubMed DOI

Dudková V., Demnerová K., Bedard D. L. (2012). Sediment-free anaerobic microbial enrichments with novel dechlorinating activity against highly chlorinated commercial PCBs. J. Chem. Technol. Biotechnol. 87, 1254–1262. 10.1002/jctb.3807 DOI

Fagervold S. K., May H. D., Sowers K. R. (2007). Microbial reductive dechlorination of Aroclor 1260 in baltimore harbor sediment microcosms is catalyzed by three phylotypes within the phylum PubMed DOI PMC

Fennell D. E., Gossett J. M., Zinder S. H. (1997). Comparison of butyric acid, ethanol, lactic acid, and propionic acid as hydrogen donors for the reductive dechlorination of tetrachloroethene. Env. Sci. Technol. 31, 918–926. 10.1021/es960756r DOI

Fennell D. E., Nijenhuis I., Wilson S. F., Zinder S. H., Häggblom M. M. (2004). PubMed DOI

Field J. A., Sierra-Alvarez R. (2008). Microbial transformation and degradation of polychlorinated biphenyls. Environ. Pollut. 155, 1–12. 10.1016/j.envpol.2007.10.016 PubMed DOI

Frame G. M., Cochran J. W., Bøwadt S. S. (1996). Complete PCB congener distributions for 17 Aroclor mixtures determined by 3 HRGC systems optimized for comprehensive, quantitative, congener-specific analysis. J. High Resolut. Chromatogr. 19, 657–668. 10.1002/jhrc.1240191202 DOI

Fuerst J. A. (2013). The PVC superphylum: exceptions to the bacterial definition? Antonie Van Leeuwenhoek 104, 451–466. 10.1007/s10482-013-9986-1 PubMed DOI

Glöckner J., Kube M., Shrestha P. M., Weber M., Glöckner F. O., Reinhardt R., et al. (2010). Phylogenetic diversity and metagenomics of candidate division OP3. Environ. Microbiol. 12, 1218–1229. 10.1111/j.1462-2920.2010.02164.x PubMed DOI

Grabic R., Hansen L. G., Ptak A., Crhova S., Gregoraszczuk E. Ł. (2006). Differential accumulation of low-chlorinated (Delor 103) and high-chlorinated (Delor 106) biphenyls in human placental tissue and opposite effects on conversion of DHEA to E2. Chemosphere 62, 573–580. 10.1016/j.chemosphere.2005.06.027 PubMed DOI

Gunsalus R. P., Romesser J. A., Wolfe R. S. (1978). Preparation of coenzyme M analogues and their activity in the methyl coenzyme M reductase system of PubMed DOI

Hiraishi A. (2008). Biodiversity of dehalorespiring bacteria with special emphasis on polychlorinated biphenyl/dioxin dechlorinators. Microbes Environ. JSME 23, 1–12. 10.1264/jsme2.23.1 PubMed DOI

Holliger C., Hahn D., Harmsen H., Ludwig W., Schumacher W., Tindall B., et al. (1998). Dehalobacter restrictus gen. nov. and sp. nov., a strictly anaerobic bacterium that reductively dechlorinates tetra- and trichloroethene in an anaerobic respiration. Arch. Microbiol. 169, 313–321. 10.1007/s002030050577 PubMed DOI

Holliger C., Kengen S. W., Schraa G., Stams A. J., Zehnder A. J. (1992). Methyl-coenzyme M reductase of PubMed PMC

Hug L. A. (2012). A Metagenome-based Examination of Dechlorinating Enrichment Cultures: Dehalococcoides and the Role of the Non-Dechlorinating Microorganisms. Doctoral Thesis University of Toronto, Toronto, Canada.

Hug L. A., Maphosa F., Leys D., Löffler F. E., Smidt H., Edwards E. A., et al. (2013). Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368, 20120322. 10.1098/rstb.2012.0322 PubMed DOI PMC

Kjellerup B. V., Paul P., Ghosh U., May H. D., Sowers K. R. (2012). Spatial distribution of PCB dechlorinating bacteria and activities in contaminated soil. Appl. Environ. Soil Sci. 2012, 1–11. 10.1155/2012/584970 DOI

Lamarche-Gagnon G., Comery R., Greer C. W., Whyte L. G. (2015). Evidence of PubMed DOI

LaRoe S. L., Fricker A. D., Bedard D. L. (2014). PubMed DOI

Mao X., Stenuit B., Polasko A., Alvarez-Cohen L. (2015). Efficient metabolic exchange and electron transfer within a syntrophic trichloroethene-degrading coculture of PubMed DOI PMC

May H. D., Miller G. S., Kjellerup B. V., Sowers K. R. (2008). Dehalorespiration with polychlorinated biphenyls by an anaerobic ultramicrobacterium. Appl. Environ. Microbiol. 74, 2089–2094. 10.1128/AEM.01450-07 PubMed DOI PMC

Meng J., Xu J., Qin D., He Y., Xiao X., Wang F. (2014). Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J. 8, 650–659. 10.1038/ismej.2013.174 PubMed DOI PMC

Oh K.-H., Ostrofsky E. B., Cho Y.-C. (2008). Molecular characterization of polychlorinated biphenyl-dechlorinating populations in contaminated sediments. J. Microbiol. Seoul Korea 46, 165–173. 10.1007/s12275-007-0214-4 PubMed DOI

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O'Hara R. B., et al. (2013). vegan: Community Ecology Package. Available online at: http://CRAN.R-project.org/package=vegan.

Passatore L., Rossetti S., Juwarkar A. A., Massacci A. (2014). Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J. Hazard. Mater. 278, 189–202. 10.1016/j.jhazmat.2014.05.051 PubMed DOI

Praveckova M., Brennerova M. V., Cvancarova M., De Alencastro L. F., Holliger C., Rossi P. (2015). Divergent PCB organohalide-respiring consortia enriched from the efflux channel of a former Delor manufacturer in Eastern Europe. Ecotoxicol. Environ. Saf. 120, 223–234. 10.1016/j.ecoenv.2015.05.038 PubMed DOI

Rinke C., Schwientek P., Sczyrba A., Ivanova N. N., Anderson I. J., Cheng J.-F., et al. (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437. 10.1038/nature12352 PubMed DOI

Rodenburg L. A., Du S., Fennell D. E., Cavallo G. J. (2010). Evidence for widespread dechlorination of polychlorinated biphenyls in groundwater, landfills, and wastewater collection systems. Environ. Sci. Technol. 44, 7534–7540. 10.1021/es1019564 PubMed DOI

Rotaru A.-E., Woodard T. L., Nevin K. P., Lovley D. R. (2015). Link between capacity for current production and syntrophic growth in Geobacter species. Front. Microbiol. 6:744 10.3389/fmicb.2015.00744 PubMed DOI PMC

Rupakula A., Lu Y., Kruse T., Boeren S., Holliger C., Smidt H., et al. (2015). Functional genomics of corrinoid starvation in the organohalide-respiring bacterium PubMed DOI PMC

Schloss P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541. 10.1128/AEM.01541-09 PubMed DOI PMC

Sung Y., Fletcher K. E., Ritalahti K. M., Apkarian R. P., Ramos-Hernandez N., Sanford R. A., et al. (2006). Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl. Environ. Microbiol. 72, 2775–2782. 10.1128/AEM.72.4.2775-2782.2006 PubMed DOI PMC

Taniyasu S., Kannan K., Holoubek I., Ansorgova A., Horii Y., Hanari N., et al. (2003). Isomer-specific analysis of chlorinated biphenyls, naphthalenes and dibenzofurans in Delor: polychlorinated biphenyl preparations from the former Czechoslovakia. Environ. Pollut. 126, 169–178. 10.1016/S0269-7491(03)00207-0 PubMed DOI

Team R. D. C. (2014). R: A Language and Environment for Statistical Computing. Vienna. Available online at: http://www.R-project.org/.

US EPA (2005). Polychlorinated Biphenyls (PCBs). Available online at: http://www3.epa.gov/epawaste/hazard/tsd/pcbs/about.html.

Wagner D. D., Hug L. A., Hatt J. K., Spitzmiller M. R., Padilla-Crespo E., Ritalahti K. M., et al. (2012). Genomic determinants of organohalide-respiration in PubMed DOI PMC

Wang S., Chng K. R., Wilm A., Zhao S., Yang K.-L., Nagarajan N., et al. (2014). Genomic characterization of three unique PubMed DOI PMC

Wang S., He J. (2013a). Dechlorination of commercial PCBs and other multiple halogenated compounds by a sediment-free culture containing PubMed DOI

Wang S., He J. (2013b). Phylogenetically distinct bacteria involve extensive dechlorination of Aroclor 1260 in sediment-free cultures. PLoS ONE 8:e59178. 10.1371/journal.pone.0059178 PubMed DOI PMC

Wu Q., Watts J. E. M., Sowers K. R., May H. D. (2002). Identification of a bacterium that specifically catalyzes the reductive dechlorination of polychlorinated biphenyls with doubly flanked chlorines. Appl. Environ. Microbiol. 68, 807–812 10.1128/aem.68.2.807-812.2002 PubMed DOI PMC

Yan J., Im J., Yang Y., Löffler F. E. (2013). Guided cobalamin biosynthesis supports PubMed DOI PMC

Yan T., LaPara T. M., Novak P. J. (2006). The reductive dechlorination of 2,3,4,5-tetrachlorobiphenyl in three different sediment cultures: evidence for the involvement of phylogenetically similar PubMed DOI PMC

Ye D., Quensen J. F., Tiedje J. M., Boyd S. A. (1992). Anaerobic dechlorination of polychlorobiphenyls (Aroclor 1242) by pasteurized and ethanol-treated microorganisms from sediments. Appl. Environ. Microbiol. 58, 1110–1114. PubMed PMC

Ye D., Quensen J. I., Tiedje J. M., Boyd S. A. (1995). Evidence for para dechlorination of polychlorobiphenyls by methanogenic bacteria. Appl. Environ. Microbiol. 61, 2166–2171. PubMed PMC

Ye D., Quensen J. I., Tiedje J. M., Boyd S. A. (1999). 2-Bromoethanesulfonate, sulfate, molybdate, and ethanesulfonate inhibit anaerobic dechlorination of polychlorobiphenyls by pasteurized microorganisms. Appl. Environ. Microbiol. 65, 327–329. PubMed PMC

Yoshida N., Ye L., Baba D., Katayama A. (2009). Reductive dechlorination of polychlorinated biphenyls and dibenzo-p-dioxins in an enrichment culture containing PubMed DOI

Zwiernik M. J., Quensen J. F., Boyd S. A. (1998). FeSO DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...