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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
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 83; Journal Issue: 8; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
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. Fri . "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},
issn = {0099-2240},
number = 8,
volume = 83,
place = {United States},
year = {2017},
month = {2}
}

Works referenced in this record:

Chlorinated Solvents in Groundwater of the United States
journal, January 2007

  • Moran, Michael J.; Zogorski, John S.; Squillace, Paul J.
  • Environmental Science & Technology, Vol. 41, Issue 1
  • DOI: 10.1021/es061553y

Chlorinated Ethene Source Remediation: Lessons Learned
journal, May 2012

  • Stroo, Hans F.; Leeson, Andrea; Marqusee, Jeffrey A.
  • Environmental Science & Technology, Vol. 46, Issue 12
  • DOI: 10.1021/es204714w

Cleaning up with genomics: applying molecular biology to bioremediation
journal, October 2003


Isolation of a Bacterium That Reductively Dechlorinates Tetrachloroethene to Ethene
journal, June 1997


Stable Carbon Isotope Fractionation of Chloroethenes by Dehalorespiring Isolates
journal, June 2007

  • Lee, Patrick K. H.; Conrad, Mark E.; Alvarez-Cohen, Lisa
  • Environmental Science & Technology, Vol. 41, Issue 12
  • DOI: 10.1021/es062763d

Versatility in Corrinoid Salvaging and Remodeling Pathways Supports Corrinoid-Dependent Metabolism in Dehalococcoides mccartyi
journal, August 2012

  • Yi, Shan; Seth, Erica C.; Men, Yu-Jie
  • Applied and Environmental Microbiology, Vol. 78, Issue 21
  • DOI: 10.1128/AEM.02150-12

Growth of a Dehalococcoides-Like Microorganism on Vinyl Chloride and cis-Dichloroethene as Electron Acceptors as Determined by Competitive PCR
journal, February 2003


Genome Sequence of the PCE-Dechlorinating Bacterium Dehalococcoides ethenogenes
journal, January 2005


Design and Verification of a Pangenome Microarray Oligonucleotide Probe Set for Dehalococcoides spp.
journal, June 2011

  • Hug, Laura A.; Salehi, Maryam; Nuin, Paulo
  • Applied and Environmental Microbiology, Vol. 77, Issue 15
  • DOI: 10.1128/AEM.00063-11

Comparative genomics of two newly isolated Dehalococcoides strains and an enrichment using a genus microarray
journal, January 2011


Identification of a Chlorobenzene Reductive Dehalogenase in Dehalococcoides sp. Strain CBDB1
journal, October 2007

  • Adrian, L.; Rahnenfuhrer, J.; Gobom, J.
  • Applied and Environmental Microbiology, Vol. 73, Issue 23
  • DOI: 10.1128/AEM.01649-07

Transcriptomic microarray analysis of corrinoid responsive genes in Dehalococcoides ethenogenes strain 195
journal, May 2009


Transcription and mass-spectroscopic proteomic studies of electron transport oxidoreductases in Dehalococcoides ethenogenes
journal, September 2006


Selective Utilization of Exogenous Amino Acids by Dehalococcoides ethenogenes Strain 195 and Its Effects on Growth and Dechlorination Activity
journal, September 2011

  • Zhuang, Wei-Qin; Yi, Shan; Feng, Xueyang
  • Applied and Environmental Microbiology, Vol. 77, Issue 21
  • DOI: 10.1128/AEM.05676-11

Investigation of Carbon Metabolism in "Dehalococcoides ethenogenes" Strain 195 by Use of Isotopomer and Transcriptomic Analyses
journal, June 2009

  • Tang, Y. J.; Yi, S.; Zhuang, W. -Q.
  • Journal of Bacteriology, Vol. 191, Issue 16
  • DOI: 10.1128/JB.00085-09

Incomplete Wood-Ljungdahl pathway facilitates one-carbon metabolism in organohalide-respiring Dehalococcoides mccartyi
journal, April 2014

  • Zhuang, W. -Q.; Yi, S.; Bill, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1321542111

Organic cofactors in the metabolism of Dehalococcoides mccartyi strains
journal, April 2013

  • Schipp, Christian J.; Marco-Urrea, Ernest; Kublik, Anja
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616
  • DOI: 10.1098/rstb.2012.0321

Phylogenetic Analysis of TCE-Dechlorinating Consortia Enriched on a Variety of Electron Donors
journal, November 2005

  • Freeborn, Ryan A.; West, Kimberlee A.; Bhupathiraju, Vishvesh K.
  • Environmental Science & Technology, Vol. 39, Issue 21
  • DOI: 10.1021/es048003p

Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides: Quantitative PCR of dechlorinating cultures
journal, December 2006


Microbial production of vitamin B 12
journal, March 2002

  • Martens, H. Barg, M. Warren, D. Jah, J. -H.
  • Applied Microbiology and Biotechnology, Vol. 58, Issue 3
  • DOI: 10.1007/s00253-001-0902-7

Unexpected Specificity of Interspecies Cobamide Transfer from Geobacter spp. to Organohalide-Respiring Dehalococcoides mccartyi Strains
journal, July 2012

  • Yan, Jun; Ritalahti, Kirsti M.; Wagner, Darlene D.
  • Applied and Environmental Microbiology, Vol. 78, Issue 18
  • DOI: 10.1128/AEM.01535-12

The corrinoid cofactor of reductive dehalogenases affects dechlorination rates and extents in organohalide-respiring Dehalococcoides mccartyi
journal, November 2015

  • Yan, Jun; Şimşir, Burcu; Farmer, Abigail T.
  • The ISME Journal, Vol. 10, Issue 5
  • DOI: 10.1038/ismej.2015.197

Influence of Vitamin B12 and Cocultures on the Growth of Dehalococcoides Isolates in Defined Medium
journal, March 2007

  • He, J.; Holmes, V. F.; Lee, P. K. H.
  • Applied and Environmental Microbiology, Vol. 73, Issue 9
  • DOI: 10.1128/AEM.02574-06

Temporal Expression of Respiratory Genes in an Enrichment Culture Containing Dehalococcoides ethenogenes
journal, August 2006

  • Rahm, B. G.; Morris, R. M.; Richardson, R. E.
  • Applied and Environmental Microbiology, Vol. 72, Issue 8
  • DOI: 10.1128/AEM.00855-06

Transcriptional Analysis of a Dehalococcoides-Containing Microbial Consortium Reveals Prophage Activation
journal, December 2011

  • Waller, Alison S.; Hug, Laura A.; Mo, Kaiguo
  • Applied and Environmental Microbiology, Vol. 78, Issue 4
  • DOI: 10.1128/AEM.06416-11

Comparative Genomics of "Dehalococcoides ethenogenes" 195 and an Enrichment Culture Containing Unsequenced "Dehalococcoides" Strains
journal, March 2008

  • West, K. A.; Johnson, D. R.; Hu, P.
  • Applied and Environmental Microbiology, Vol. 74, Issue 11
  • DOI: 10.1128/AEM.01835-07

Global gene expression of Dehalococcoides within a robust dynamic TCE-dechlorinating community under conditions of periodic substrate supply
journal, February 2013

  • West, Kimberlee A.; Lee, Patrick K. H.; Johnson, David R.
  • Biotechnology and Bioengineering, Vol. 110, Issue 5
  • DOI: 10.1002/bit.24819

Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes
journal, March 2015

  • Hultman, Jenni; Waldrop, Mark P.; Mackelprang, Rachel
  • Nature, Vol. 521, Issue 7551
  • DOI: 10.1038/nature14238

Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill
journal, June 2012

  • Mason, Olivia U.; Hazen, Terry C.; Borglin, Sharon
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.59

Microbial community gene expression in ocean surface waters
journal, March 2008

  • Frias-Lopez, J.; Shi, Y.; Tyson, G. W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 10
  • DOI: 10.1073/pnas.0708897105

Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage
journal, December 2014


A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer
journal, March 2013

  • Ishii, Shun’ichi; Suzuki, Shino; Norden-Krichmar, Trina M.
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2615

Metagenomic analysis of a stable trichloroethene-degrading microbial community
journal, March 2012

  • Brisson, Vanessa L.; West, Kimberlee A.; Lee, Patrick KH
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.15

Microbial ecology of chlorinated solvent biodegradation: Microbial ecology of PCE degradation
journal, March 2014

  • David, Maude M.; Cecillon, Sebastien; Warne, Brett M.
  • Environmental Microbiology, Vol. 17, Issue 12
  • DOI: 10.1111/1462-2920.12413

Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013

  • Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
  • Nature Biotechnology, Vol. 31, Issue 6
  • DOI: 10.1038/nbt.2579

Characterization of four TCE-dechlorinating microbial enrichments grown with different cobalamin stress and methanogenic conditions
journal, May 2013

  • Men, Yujie; Lee, Patrick K. H.; Harding, Katie C.
  • Applied Microbiology and Biotechnology, Vol. 97, Issue 14
  • DOI: 10.1007/s00253-013-4896-8

The Many Faces of Vitamin B12: Catalysis by Cobalamin-Dependent Enzymes
journal, June 2003


Identification of phenolyl cobamide from the homoacetogenic bacterium Sporomusa ovata
journal, December 1989


Sustainable Growth of Dehalococcoides mccartyi 195 by Corrinoid Salvaging and Remodeling in Defined Lactate-Fermenting Consortia
journal, January 2014

  • Men, Yujie; Seth, Erica C.; Yi, Shan
  • Applied and Environmental Microbiology, Vol. 80, Issue 7
  • DOI: 10.1128/AEM.03477-13

Tetrachloromethane-Degrading Bacterial Enrichment Cultures and Isolates from a Contaminated Aquifer
journal, July 2015


Identification of microorganisms involved in reductive dehalogenation of chlorinated ethenes in an anaerobic microbial community
journal, October 2005


Nutrient cross-feeding in the microbial world
journal, July 2014


Nocturnal Production of Endospores in Natural Populations of Epulopiscium-Like Surgeonfish Symbionts
journal, October 2005


Updates on the sporulation process in Clostridium species
journal, May 2015

  • Talukdar, Prabhat K.; Olguín-Araneda, Valeria; Alnoman, Maryam
  • Research in Microbiology, Vol. 166, Issue 4
  • DOI: 10.1016/j.resmic.2014.12.001

Recent progress in Bacillus subtilis sporulation
journal, January 2012


Anaerobic biosynthesis of the lower ligand of vitamin B 12
journal, August 2015

  • Hazra, Amrita B.; Han, Andrew W.; Mehta, Angad P.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 34
  • DOI: 10.1073/pnas.1509132112

Linear amplification for deep sequencing
journal, June 2011

  • Hoeijmakers, Wieteke A. M.; Bártfai, Richárd; Françoijs, Kees-Jan
  • Nature Protocols, Vol. 6, Issue 7
  • DOI: 10.1038/nprot.2011.345

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

    Works referencing / citing this record:

    Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
    journal, July 2019


    Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
    journal, July 2019