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Analysis and Comparison of the Microbial Community Structures of Two Enrichment Cultures Capable of Reductively Dechlorinating TCE and Cis-DCE

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Analysis and Comparison of the Microbial Community Structures of Two Enrichment Cultures Capable of Reductively Dechlorinating TCE and Cis-DCE Blackwell Science, LtdOxford, UKEMIEnvironmental Microbiology 1462-2920Society for Applied Microbiology and Blackwell Publishing Ltd, 2003614554Original ArticleA. Z. Gu et al. Environmental Microbiology (2004) 6(1), 45–54 doi:10.1046/j.1462-2920.2003.00525.x Analysis and comparison of the microbial community structures of two enrichment cultures capable of reductively dechlorinating TCE and cis-DCE April Z. Gu,1* Brian P. Hedlund,2,4 James T. Staley,2 organism closely related to Dehalococcoides etheno- Stuart E. Strand3 and H. David Stensel1 genes to be the presumptive dechlorinator in both 1Department of Civil and Environmental engineering, enrichments. Different electron acceptors affected the University of Washington, Seattle, WA 98195, USA. bacterial diversity and the community profiles of the 2Department of Microbiology, University of Washington, two enrichments. Most of the sequences identified in Seattle, WA 98195, USA. our dechlorinating enrichments shared high similari- 3College of Forest Resources, University of Washington, ties with sequences previously obtained from other Seattle, WA 98195, USA. enriched dechlorinating cultures and chlorinated- 4Department of Biological Sciences, University of Nevada, compound-contaminated sediments or aquifers, sug- Las Vegas, NV 89154–4004, USA. gesting these bacteria may have direct or indirect roles in reductive dechlorination. Summary Introduction In order to study the effect of different chloroethenes (electron acceptors) on the bacterial composition of The toxic chlorinated solvents PCE and TCE are among dechlorinating communities, two reductive dechlori- the most abundant groundwater contaminants. Under nating enrichment cultures were developed that were anaerobic conditions, PCE or TCE can be sequentially able to reduce trichloroethene (TCE) and cis-1,2- reduced to cis-DCE or to vinyl chloride (VC) and ethene dichloroethene (cis-DCE) to ethene using hydrogen by energy-yielding dehalorespiration or by cometabolic as electron donor, respectively. The inoculum for the processes (Middeldorp et al., 1999). Because the reduc- cultures was material from a methanogenic fluidized tive dehalogenation of PCE and TCE in respiratory pro- bed reactor (FBR), which was originally seeded with cesses is faster than anaerobic cometabolic processes, digester sludge and showed a stable capacity for tet- and because anaerobic conditions usually prevail in aqui- rachloroethene (PCE) reduction to ethene for over six fers, reductive dechlorination has been the most studied years. Molecular methods were used to determine and and applied approach for bioremediation of PCE or TCE compare the microbial communities of these two contaminated aquifers. enrichment cultures. A clone library of bacterial 16S The reductive dechlorination process usually occurs in rRNA genes was generated for each enrichment. The environments where methanogenesis and/or acetogene- clones were screened into different groups by restric- sis occurs (Holliger et al., 1999). The dechlorination func- tion fragment length polymorphism (RFLP) analysis tion of a chloroethene-reducing microbial consortium, like using two different four base pair recognition restric- any other anaerobic ecosystem, relies on the biochemical tion enzymes. A total of 12 sequence types were iden- collaboration of different members in the microbial com- tified by phylogenetic analysis of nearly complete 16S munity. Many mixed cultures have been described that rDNA sequences (~1450 bp). The sequences were exhibit stable capacities to reduce chloroethenes com- affiliated with six recognized phyla of the domain Bac- pletely to ethene after several laboratory transfers or dur- teria: Firmicutes (low G+C Gram-positives), Chlorof- ing long-term performance in continuously operated lexi (green non-sulphur bacteria), Actinobacteria reactors (Vogel and McCarty, 1985; DiStefano et al., (high G+C Gram-positives), Bacteroidetes (Cytoph- 1991; Debruin et al., 1992; Holliger et al., 1993; Balla- aga-Flexibacter-Bacteroides), Nitrospira and Spiro- pragada et al., 1997; Flynn et al., 2000). However, the chaetes. The results led to the identification of an microbial compositions of such chloroethene-dehaloge- nating communities have not been studied extensively. Most studies of chlorinated-ethene-dehalorespiring Received 28 April, 2003; accepted 27 August, 2003. *For correspon- dence. E-mail [email protected]; Tel. (+1) 206 543 0785; Fax organisms have been based on traditional isolation- (+1) 206 685 9185. dependent methods, and have found that chlorinated- © 2004 Blackwell Publishing Ltd 46 A. Z. Gu et al. ethene-dehalorespiring organisms can be categorized ethene. Because reductive dechlorination can occur in the into two groups (Middeldorp et al., 1999). One physiolog- absence of methanogens (DiStefano et al., 1991) and all ical group, which reductively dechlorinates PCE and TCE known chloroethene-respiring organisms belong to the only to cis-DCE, includes phylogenetically diverse groups domain Bacteria, only the bacterial community was char- of bacteria that lie in the Firmicutes, or d and e branches acterized in this study. Possible roles of some populations of the Proteobacteria. Another group, which is capable of present in the enrichments are discussed. further reductive dechlorination of cis-DCE to VC and ethene, is a specific cluster of bacteria that is closely related to Dehalococcoides ethenogenes, lying within the Results and discussion Chloroflexi (green non-sulphur bacteria). Isolation of Establishment of the TCE- and cis-DCE-dechlorinating dechlorinators that are capable of reducing cis-DCE or VC cultures to ethene has been difficult (Ballapragada et al., 1997; Cupples et al., 2003). Dehalococcoides ethenogenes Two methanogenic subculture enrichments were estab- strain 195 and Dehalococcoides sp. strain FL2 are the lished, one degrading TCE to ethene and the other only known isolates that are able to completely reduce degrading cis-DCE to ethene. The enrichments were PCE to ethene. However, unknown growth factors within inoculated with material from a methanogenic, PCE- a sludge supernatant are required by strain 195, suggest- degrading FBR culture, which was originally seeded with ing that the dechlorinators may have a syntrophic interac- activated sludge (Ballapragada et al., 1997), and was tion with other organisms in the consortium (Maymo- able to carry out complete reductive dechlorination of Gatell et al., 1997). Even though the Dehalococcoides PCE or TCE to ethene in the temperature range of 15– group is often detected in environmental samples that 35∞C (Pietari, 1999). H2 was found to be the direct elec- perform complete dechlorination of chloroethenes (Löffler tron donor for the reduction of chlorinated compounds. et al., 2000; Fennell et al., 2001; Hohnstock-Ashe et al., For the development of subcultures, lactate was used as 2001; Hendrickson et al., 2002), it still remains to be seen the electron donor and carbon source initially. Dechlori- whether there are other organisms in the environment that nation activity started after about 3–4 weeks. Later, lac- can catalyse the dechlorination of PCE or TCE to ethene tate was replaced with H2 as the electron donor and besides Dehalococcoides. acetate as the carbon source to simplify the community. A limited knowledge of dechlorinating microorganisms The reductive dechlorination rates slowly increased and and of the diversity of microorganisms involved in the seem to be stabilized after 6 months. After enrichment for dehalogenation processes often hampers the understand- over 8 months, the biomass concentrations (as volatile ing and the application of the complete reductive dechlo- suspended solids, VSS) of the two enrichment cultures rination technology for bioremediation of chlorinated increased to about 300 mg l-1 and 500 mg l-1 for the cis- ethenes. Fundamental information on the ecology and DCE and TCE-reducing culture respectively. Methane biophysical interaction of community members involved in was produced in both cultures. The TCE-fed subculture the partial and complete dechlorination processes should was intended to enrich for bacteria carrying out reductive help to better understand and design successful remedi- dechlorination of TCE to cis-DCE and for bacteria carry- ation strategies for different chloroethene-contaminated ing out complete reductive dechlorination of TCE to sites. ethene. The cis-DCE fed culture was intended to enrich Culture-independent, 16S rDNA-based molecular for only bacteria that were able to carry reductive dechlo- approaches have been useful in studying microbial diver- rination of cis-DCE to ethene. However, after 8 months sity and community structure of mixed enrichment cul- exposure to only cis-DCE, the cis-DCE-fed culture was tures. Molecular methods have been applied to conduct still able to reduce TCE. phylogenetic analyses of a number of consortia that deh- alogenate chlorinated aromatic compounds (Adrian et al., Chloroethene degradation characteristics of the 1998; Pulliam-Holoman et al., 1998; von Wintzingerode enrichments et al., 1999; Zhou et al., 1999; Breitenstein et al., 2001). However, only a few microbial community analysis studies Degradation of TCE and cis-DCE and formation of corre- have been conducted with chloroethene-reducing enrich- sponding dechlorination intermediate products by the ments or ecosystems (Dojka et al., 1998; Richardson TCE-reducing and cis-DCE-reducing enrichment cultures et al., 2002). are shown in Fig. 1. Conversions of TCE
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