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
The aim of this paper is to obtain a systems-level understanding of the interactions between Dehalococcoides and 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 the Veillonellaceae bin-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 corrinoid de novo biosynthesis pathway was also assigned to the Veillonellaceae bin-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 of Dehalococcoides was upregulated in response to the cobalamin stress. Finally, this study provides important insights into the microbial interactionsmore »
- Authors:
-
- Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of California, Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
- National Research Council Canada, Montreal, QC (Canada)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of Hong Kong (China)
- Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Inst. of Health (NIH) (United States); Danish Research Council (Denmark)
- OSTI Identifier:
- 1379788
- Grant/Contract Number:
- AC02-05CH11231; CBET-1336709; S10RR029668; S10RR027303; R42 ES004705-19; R01 ES024255-01; 09-069890
- Resource Type:
- Accepted Manuscript
- 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:
- 59 BASIC BIOLOGICAL SCIENCES; 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, and Alvarez-Cohen, Lisa. 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. 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. https://doi.org/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, and Alvarez-Cohen, Lisa. 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. https://doi.org/10.1128/AEM.03508-16. https://www.osti.gov/servlets/purl/1379788.
@article{osti_1379788,
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},
abstractNote = {The aim of this paper is to obtain a systems-level understanding of the interactions between Dehalococcoides and 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 the Veillonellaceae bin-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 corrinoid de novo biosynthesis pathway was also assigned to the Veillonellaceae bin-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 of Dehalococcoides was upregulated in response to the cobalamin stress. Finally, this study provides important insights into the microbial interactions and roles played by members of dechlorinating communities under cobalamin-limited conditions.},
doi = {10.1128/AEM.03508-16},
journal = {Applied and Environmental Microbiology},
number = 8,
volume = 83,
place = {United States},
year = {Fri Feb 10 00:00:00 EST 2017},
month = {Fri Feb 10 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
Comparative genomics of two newly isolated Dehalococcoides strains and an enrichment using a genus microarray
journal, January 2011
- Lee, Patrick K. H.; Cheng, Dan; Hu, Ping
- The ISME Journal, Vol. 5, Issue 6
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
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
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
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
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
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
Nutrient cross-feeding in the microbial world
journal, July 2014
- Seth, Erica C.; Taga, Michiko E.
- Frontiers in Microbiology, Vol. 5
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
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
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
Cleaning up with genomics: applying molecular biology to bioremediation
journal, October 2003
- Lovley, Derek R.
- Nature Reviews Microbiology, Vol. 1, Issue 1
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
Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides: Quantitative PCR of dechlorinating cultures
journal, December 2006
- Duhamel, Melanie; Edwards, Elizabeth A.
- FEMS Microbiology Ecology, Vol. 58, Issue 3, p. 538-549
Chlorinated Ethene Source Remediation: Lessons Learned
journal, May 2012
- Stroo, Hans F.; Leeson, Andrea; Marqusee, Jeffrey A.
- Environmental Science & Technology, Vol. 46, Issue 12
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
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
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
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
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
Linear amplification for deep sequencing
journal, June 2011
- Hoeijmakers, Wieteke A. M.; Bártfai, Richárd; Françoijs, Kees-Jan
- Nature Protocols, Vol. 6, Issue 7
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
Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi
journal, April 2012
- Loffler, F. E.; Yan, J.; Ritalahti, K. M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2
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
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
The Many Faces of Vitamin B12: Catalysis by Cobalamin-Dependent Enzymes
journal, June 2003
- Banerjee, Ruma; Ragsdale, Stephen W.
- Annual Review of Biochemistry, Vol. 72, Issue 1, p. 209-247
Isolation of a Bacterium That Reductively Dechlorinates Tetrachloroethene to Ethene
journal, June 1997
- Maymo-Gatell, X.
- Science, Vol. 276, Issue 5318
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
Transcriptomic microarray analysis of corrinoid responsive genes in Dehalococcoides ethenogenes strain 195
journal, May 2009
- Johnson, David R.; Nemir, Audra; Andersen, Gary L.
- FEMS Microbiology Letters, Vol. 294, Issue 2
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
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
Comparative metagenomic and metatranscriptomic analyses of microbial communities in acid mine drainage
journal, December 2014
- Chen, Lin-xing; Hu, Min; Huang, Li-nan
- The ISME Journal, Vol. 9, Issue 7
A History of the Production and Use of Carbon Tetrachloride, Tetrachloroethylene, Trichloroethylene and 1,1,1-Trichloroethane in the United States: Part 1--Historical Background; Carbon Tetrachloride and Tetrachloroethylene
journal, January 2000
- Doherty, Richard E.
- Environmental Forensics, Vol. 1, Issue 2
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
Identification of phenolyl cobamide from the homoacetogenic bacterium Sporomusa ovata
journal, December 1989
- Stupperich, Erhard; Eisinger, Hans Jurgen; KRaTLER, Bernhard
- European Journal of Biochemistry, Vol. 186, Issue 3
Tetrachloromethane-Degrading Bacterial Enrichment Cultures and Isolates from a Contaminated Aquifer
journal, July 2015
- Penny, Christian; Gruffaz, Christelle; Nadalig, Thierry
- Microorganisms, Vol. 3, Issue 3
Complete Detoxification of Vinyl Chloride by an Anaerobic Enrichment Culture and Identification of the Reductively Dechlorinating Population as a Dehalococcoides Species
journal, February 2003
- He, J.; Ritalahti, K. M.; Aiello, M. R.
- Applied and Environmental Microbiology, Vol. 69, Issue 2
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
Transcription and mass-spectroscopic proteomic studies of electron transport oxidoreductases in Dehalococcoides ethenogenes
journal, September 2006
- Morris, R. M.; Sowell, S.; Barofsky, D.
- Environmental Microbiology, Vol. 8, Issue 9
Recent progress in Bacillus subtilis sporulation
journal, January 2012
- Higgins, Douglas; Dworkin, Jonathan
- FEMS Microbiology Reviews, Vol. 36, Issue 1
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
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
Molecular Characterization of a Dechlorinating Community Resulting from In Situ Biostimulation in a Trichloroethene-Contaminated Deep, Fractured Basalt Aquifer and Comparison to a Derivative Laboratory Culture
journal, December 2004
- Macbeth, T. W.; Cummings, D. E.; Spring, S.
- Applied and Environmental Microbiology, Vol. 70, Issue 12
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
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
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
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
Genome Sequence of the PCE-Dechlorinating Bacterium Dehalococcoides ethenogenes
journal, January 2005
- Seshadri, R.
- Science, Vol. 307, Issue 5706
Identification of microorganisms involved in reductive dehalogenation of chlorinated ethenes in an anaerobic microbial community
journal, October 2005
- Yang, Yanru; Pesaro, Manuel; Sigler, William
- Water Research, Vol. 39, Issue 16
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
Nocturnal Production of Endospores in Natural Populations of Epulopiscium-Like Surgeonfish Symbionts
journal, October 2005
- Flint, J. F.; Drzymalski, D.; Montgomery, W. L.
- Journal of Bacteriology, Vol. 187, Issue 21
Identification of specific corrinoids reveals corrinoid modification in dechlorinating microbial communities: Corrinoids in dechlorinating communities
journal, June 2014
- Men, Yujie; Seth, Erica C.; Yi, Shan
- Environmental Microbiology, Vol. 17, Issue 12
Growth of a Dehalococcoides-Like Microorganism on Vinyl Chloride and cis-Dichloroethene as Electron Acceptors as Determined by Competitive PCR
journal, February 2003
- Cupples, A. M.; Spormann, A. M.; McCarty, P. L.
- Applied and Environmental Microbiology, Vol. 69, Issue 2
Works referencing / citing this record:
Synthetic microbial consortia for biosynthesis and biodegradation: promises and challenges
journal, July 2019
- Che, Shun; Men, Yujie
- Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10
Growth of Dehalococcoides mccartyi species in an autotrophic consortium producing limited acetate
journal, August 2018
- Ding, Chang; Alvarez-Cohen, Lisa; He, Jianzhong
- Biodegradation, Vol. 29, Issue 5
Sustained Dechlorination of Vinyl Chloride to Ethene in Dehalococcoides -Enriched Cultures Grown without Addition of Exogenous Vitamins and at Low pH
journal, August 2019
- Puentes Jácome, Luz A.; Wang, Po-Hsiang; Molenda, Olivia
- Environmental Science & Technology, Vol. 53, Issue 19
An integrative overview of genomic, transcriptomic and proteomic analyses in organohalide respiration research
journal, January 2018
- Türkowsky, Dominique; Jehmlich, Nico; Diekert, Gabriele
- FEMS Microbiology Ecology, Vol. 94, Issue 3
An integrated meta-omics approach reveals substrates involved in synergistic interactions in a bisphenol A (BPA)-degrading microbial community
journal, February 2019
- Yu, Ke; Yi, Shan; Li, Bing
- Microbiome, Vol. 7, Issue 1