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Title: Metagenomic and Metatranscriptomic Analyses Reveal the Structure and Dynamics of a Dechlorinating Community Containing Dehalococcoides mccartyi and Corrinoid-Providing Microorganisms under Cobalamin-Limited Conditions

Abstract

ABSTRACT The aim of this study is to obtain a systems-level understanding of the interactions betweenDehalococcoidesand corrinoid-supplying microorganisms by analyzing community structures and functional compositions, activities, and dynamics in trichloroethene (TCE)-dechlorinating enrichments. Metagenomes and metatranscriptomes of the dechlorinating enrichments with and without exogenous cobalamin were compared. Seven putative draft genomes were binned from the metagenomes. At an early stage (2 days), more transcripts of genes in theVeillonellaceaebin-genome were detected in the metatranscriptome of the enrichment without exogenous cobalamin than in the one with the addition of cobalamin. Among these genes, sporulation-related genes exhibited the highest differential expression when cobalamin was not added, suggesting a possible release route of corrinoids from corrinoid producers. Other differentially expressed genes include those involved in energy conservation and nutrient transport (including cobalt transport). The most highly expressed corrinoidde novobiosynthesis pathway was also assigned to theVeillonellaceaebin-genome. Targeted quantitative PCR (qPCR) analyses confirmed higher transcript abundances of those corrinoid biosynthesis genes in the enrichment without exogenous cobalamin than in the enrichment with cobalamin. Furthermore, the corrinoid salvaging and modification pathway ofDehalococcoideswas upregulated in response to the cobalamin stress. This study provides important insights into the microbial interactions and roles played by members of dechlorinating communities under cobalamin-limitedmore » conditions. IMPORTANCEThe key chloroethene-dechlorinating bacteriumDehalococcoides mccartyiis a cobalamin auxotroph, thus acquiring corrinoids from other community members. Therefore, it is important to investigate the microbe-microbe interactions betweenDehalococcoidesand the corrinoid-providing microorganisms in a community. This study provides systems-level information, i.e., taxonomic and functional compositions and dynamics of the supportive microorganisms in dechlorinating communities under different cobalamin conditions. The findings shed light on the important roles ofVeillonellaceaespecies in the communities compared to other coexisting community members in producing and providing corrinoids forDehalococcoidesspecies under cobalamin-limited conditions.« less

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1372982
Report Number(s):
PNNL-SA-126554
Journal ID: ISSN 0099-2240
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Applied and Environmental Microbiology; Journal Volume: 83; Journal Issue: 8
Country of Publication:
United States
Language:
English
Subject:
Dehalococcoides; reductive dechlorination; corrinoid; Veillonellaceae; metagenome; metatranscriptome

Citation Formats

Men, Yujie, Yu, Ke, Bælum, Jacob, Gao, Ying, Tremblay, Julien, Prestat, Emmanuel, Stenuit, Ben, Tringe, Susannah G., Jansson, Janet, Zhang, Tong, Alvarez-Cohen, Lisa, and Liu, Shuang-Jiang. Metagenomic and Metatranscriptomic Analyses Reveal the Structure and Dynamics of a Dechlorinating Community Containing Dehalococcoides mccartyi and Corrinoid-Providing Microorganisms under Cobalamin-Limited Conditions. United States: N. p., 2017. Web. doi:10.1128/AEM.03508-16.
Men, Yujie, Yu, Ke, Bælum, Jacob, Gao, Ying, Tremblay, Julien, Prestat, Emmanuel, Stenuit, Ben, Tringe, Susannah G., Jansson, Janet, Zhang, Tong, Alvarez-Cohen, Lisa, & Liu, Shuang-Jiang. Metagenomic and Metatranscriptomic Analyses Reveal the Structure and Dynamics of a Dechlorinating Community Containing Dehalococcoides mccartyi and Corrinoid-Providing Microorganisms under Cobalamin-Limited Conditions. United States. doi:10.1128/AEM.03508-16.
Men, Yujie, Yu, Ke, Bælum, Jacob, Gao, Ying, Tremblay, Julien, Prestat, Emmanuel, Stenuit, Ben, Tringe, Susannah G., Jansson, Janet, Zhang, Tong, Alvarez-Cohen, Lisa, and Liu, Shuang-Jiang. 2017. "Metagenomic and Metatranscriptomic Analyses Reveal the Structure and Dynamics of a Dechlorinating Community Containing Dehalococcoides mccartyi and Corrinoid-Providing Microorganisms under Cobalamin-Limited Conditions". United States. doi:10.1128/AEM.03508-16.
@article{osti_1372982,
title = {Metagenomic and Metatranscriptomic Analyses Reveal the Structure and Dynamics of a Dechlorinating Community Containing Dehalococcoides mccartyi and Corrinoid-Providing Microorganisms under Cobalamin-Limited Conditions},
author = {Men, Yujie and Yu, Ke and Bælum, Jacob and Gao, Ying and Tremblay, Julien and Prestat, Emmanuel and Stenuit, Ben and Tringe, Susannah G. and Jansson, Janet and Zhang, Tong and Alvarez-Cohen, Lisa and Liu, Shuang-Jiang},
abstractNote = {ABSTRACT The aim of this study is to obtain a systems-level understanding of the interactions betweenDehalococcoidesand corrinoid-supplying microorganisms by analyzing community structures and functional compositions, activities, and dynamics in trichloroethene (TCE)-dechlorinating enrichments. Metagenomes and metatranscriptomes of the dechlorinating enrichments with and without exogenous cobalamin were compared. Seven putative draft genomes were binned from the metagenomes. At an early stage (2 days), more transcripts of genes in theVeillonellaceaebin-genome were detected in the metatranscriptome of the enrichment without exogenous cobalamin than in the one with the addition of cobalamin. Among these genes, sporulation-related genes exhibited the highest differential expression when cobalamin was not added, suggesting a possible release route of corrinoids from corrinoid producers. Other differentially expressed genes include those involved in energy conservation and nutrient transport (including cobalt transport). The most highly expressed corrinoidde novobiosynthesis pathway was also assigned to theVeillonellaceaebin-genome. Targeted quantitative PCR (qPCR) analyses confirmed higher transcript abundances of those corrinoid biosynthesis genes in the enrichment without exogenous cobalamin than in the enrichment with cobalamin. Furthermore, the corrinoid salvaging and modification pathway ofDehalococcoideswas upregulated in response to the cobalamin stress. This study provides important insights into the microbial interactions and roles played by members of dechlorinating communities under cobalamin-limited conditions. IMPORTANCEThe key chloroethene-dechlorinating bacteriumDehalococcoides mccartyiis a cobalamin auxotroph, thus acquiring corrinoids from other community members. Therefore, it is important to investigate the microbe-microbe interactions betweenDehalococcoidesand the corrinoid-providing microorganisms in a community. This study provides systems-level information, i.e., taxonomic and functional compositions and dynamics of the supportive microorganisms in dechlorinating communities under different cobalamin conditions. The findings shed light on the important roles ofVeillonellaceaespecies in the communities compared to other coexisting community members in producing and providing corrinoids forDehalococcoidesspecies under cobalamin-limited conditions.},
doi = {10.1128/AEM.03508-16},
journal = {Applied and Environmental Microbiology},
number = 8,
volume = 83,
place = {United States},
year = 2017,
month = 2
}
  • We present a statistical model designed to identify the effect of experimental perturbations on the aggregate behavior of the transcriptome expressed by the bacterium Dehalococcoides mccartyi strain 195. Strains of Dehalococcoides are used in sub-surface bioremediation applications because they organohalorespire tetrachloroethene and trichloroethene (common chlorinated solvents that contaminate the environment) to non-toxic ethene. However, the biochemical mechanism of this process remains incompletely described. Additionally, the response of Dehalococcoides to stress-inducing conditions that may be encountered at field-sites is not well understood. The constructed statistical model captured the aggregate behavior of gene expression phenotypes by modeling the distinct eigengenes of 100more » transcript clusters, determining stable relationships among these clusters of gene transcripts with a sparse network-inference algorithm, and directly modeling the effect of changes in experimental conditions by constructing networks conditioned on the experimental state. Based on the model predictions, we discovered new response mechanisms for DMC, notably when the bacterium is exposed to solvent toxicity. The network identified a cluster containing thirteen gene transcripts directly connected to the solvent toxicity condition. Transcripts in this cluster include an iron-dependent regulator (DET0096-97) and a methylglyoxal synthase (DET0137). To validate these predictions, additional experiments were performed. Continuously fed cultures were exposed to saturating levels of tetrachloethene, thereby causing solvent toxicity, and transcripts that were predicted to be linked to solvent toxicity were monitored by quantitative reverse-transcription polymerase chain reaction. Twelve hours after being shocked with saturating levels of tetrachloroethene, the control transcripts (encoding for a key hydrogenase and the 16S rRNA) did not significantly change. By contrast, transcripts for DET0137 and DET0097 displayed a 46.8±11.5 and 14.6±9.3 fold up-regulation, respectively, supporting the model. This is the first study to identify transcripts in Dehalococcoides that potentially respond to tetrachloroethene solvent-toxicity conditions that may be encountered near contamination source zones in sub-surface environments.« less
  • The influence of dechlorinating microorganisms on PCE and its reduced end products in the presence of a PCE-containing nonaqueous phase liquid (NAPL) was investigated. Experiments were conducted in continuous-flow stirred-tank reactors (CFSTRs) containing a mixed PCE dechlorinating culture and a model NAPL consisting of PCE and tridecane. Comparisons between biotic and abiotic CFSTRs demonstrated that dechlorination resulted in a factor of 14 increase in PCE removal rates from the NAPL. The formation of dechlorination daughter products trichloroethene and cis-dichloroethene were observed, and cis-dichloroethene was not dechlorinated further. Partitioning of daughter products between phases caused temporal changes in the chlorinated ethenesmore » distribution within the NAPL. The combined effects of dissolution and dechlorination on the removal of chlorinated ethenes from the NAPL were described using a mathematical model that approximated dechlorination as a pseudo-first-order process. Pseudo-first-order dechlorination rate coefficients for PCE and TCE were determined and were 0.18 and 0.27 h{sup {minus}1}, respectively. It was determined that total chlorinated ethenes removal from the NAPL would be achieved in 13 days in biotic CFSTRs, as compared to 77 days in the abiotic CFSTRs--corresponding to an 83% reduction in longevity of the chlorinated ethenes component of the NAPL.« less
  • Members of the genera Desulfuromonas and Dehalococcoides reductively dechlorinate tetrachloroethene (PCE) and trichloroethene. Two primer pairs specific to hypervariable regions of the 16S rRNA genes of the Dehalococcoides group (comprising Dehalococcoides ethenogenes and Dehalococcoides sp. strain FL2) and the acetate-oxidizing, PCE-dechlorinating Desulfuromonas group (comprising Desulfuromonas sp. strain BB1 and Desulfuromonas chloroethenica) were designed. The detection threshold of a nested PCR approach using universal bacterial primers followed by a second PCR with the Desulfuromonas dechlorinator-targeted primer pair was 1 x 10{sup 3} BB1 cells added per gram (wet weight) of sandy aquifer material. Total community DNA isolated from sediments of threemore » Michigan rivers and six different chloroethene-contaminated aquifer samples was used as template in nested PCR. All river sediment samples yielded positive signals with the BB1- and the Dehalococcoides-targeted primers. One chloroethene-contaminated aquifer tested positive with the Dehalococcoides-targeted primers, and another contaminated aquifer tested positive with the Desulfuromonas dechlorinator-targeted primer pair. Restriction fragment analysis of the amplicons could discriminate strain BB1 from other known Desulfuromonas species. Microcosm studies confirmed the presence of PCE-dechlorinating, acetate-oxidizing Desulfuromonas and hydrogenotrophic Dehalococcoides species in samples yielding positive PCR signals with the specific primers.« less