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Title: Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes

Abstract

Here, organohalide-respiring bacteria play key roles in the natural chlorine cycle; however, most of the current knowledge is based on cultures from contaminated environments. We demonstrate that grape pomace compost without prior exposure to chlorinated solvents harbors a Dehalogenimonas ( Dhgm) species capable of using chlorinated ethenes, including the human carcinogen and common groundwater pollutant vinyl chloride (VC) as electron acceptors. Grape pomace microcosms and derived solid-free enrichment cultures were able to dechlorinate trichloroethene (TCE) to less chlorinated daughter products including ethene. 16S rRNA gene amplicon and qPCR analyses revealed the predominance of Dhgm sequences, but no Dehalococcoides mccartyi ( Dhc) biomarker genes were detected. The enumeration of Dhgm 16S rRNA genes demonstrated VC-dependent growth, and 6.55 ± 0.64 x 10 8 cells were produced per µmole of chloride released. Metagenome sequencing enabled the assembly of a Dhgm draft genome, and 52 putative reductive dehalogenase (RDase) genes were identified. Proteomic workflows identified a putative VC RDase with 49% and 56.1% amino acid similarity to the known VC RDases VcrA and BvcA, respectively. A survey of 1,173 groundwater samples collected from 111 chlorinated solvent-contaminated sites revealed that Dhgm 16S rRNA genes were frequently detected and outnumbered Dhc in 65% of themore » samples. Dhgm may be more relevant contributors to chlorinated solvent reductive dechlorination in contaminated aquifers than is currently recognized, and non-polluted environments are a source of strictly organohalide-respiring bacteria with novel RDase genes.« less

Authors:
 [1];  [1];  [2];  [3];  [4]; ORCiD logo [5]; ORCiD logo [5];  [6];  [6]; ORCiD logo [1]
  1. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Chinese Academy of Sciences, Liaoning (China)
  3. Univ. of Tennessee, Knoxville, TN (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  6. Microbial Insights, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1408046
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; 54 ENVIRONMENTAL SCIENCES

Citation Formats

Yang, Yi, Higgins, Steven A., Yan, Jun, Şimşir, Burcu, Chourey, Karuna, Iyer, Ramsunder M., Hettich, Robert L., Baldwin, Brett, Ogles, Dora M., and Loffler, Frank E. Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes. United States: N. p., 2017. Web. doi:10.1038/ismej.2017.127.
Yang, Yi, Higgins, Steven A., Yan, Jun, Şimşir, Burcu, Chourey, Karuna, Iyer, Ramsunder M., Hettich, Robert L., Baldwin, Brett, Ogles, Dora M., & Loffler, Frank E. Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes. United States. doi:10.1038/ismej.2017.127.
Yang, Yi, Higgins, Steven A., Yan, Jun, Şimşir, Burcu, Chourey, Karuna, Iyer, Ramsunder M., Hettich, Robert L., Baldwin, Brett, Ogles, Dora M., and Loffler, Frank E. Tue . "Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes". United States. doi:10.1038/ismej.2017.127. https://www.osti.gov/servlets/purl/1408046.
@article{osti_1408046,
title = {Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes},
author = {Yang, Yi and Higgins, Steven A. and Yan, Jun and Şimşir, Burcu and Chourey, Karuna and Iyer, Ramsunder M. and Hettich, Robert L. and Baldwin, Brett and Ogles, Dora M. and Loffler, Frank E.},
abstractNote = {Here, organohalide-respiring bacteria play key roles in the natural chlorine cycle; however, most of the current knowledge is based on cultures from contaminated environments. We demonstrate that grape pomace compost without prior exposure to chlorinated solvents harbors a Dehalogenimonas (Dhgm) species capable of using chlorinated ethenes, including the human carcinogen and common groundwater pollutant vinyl chloride (VC) as electron acceptors. Grape pomace microcosms and derived solid-free enrichment cultures were able to dechlorinate trichloroethene (TCE) to less chlorinated daughter products including ethene. 16S rRNA gene amplicon and qPCR analyses revealed the predominance of Dhgm sequences, but no Dehalococcoides mccartyi (Dhc) biomarker genes were detected. The enumeration of Dhgm 16S rRNA genes demonstrated VC-dependent growth, and 6.55 ± 0.64 x 108 cells were produced per µmole of chloride released. Metagenome sequencing enabled the assembly of a Dhgm draft genome, and 52 putative reductive dehalogenase (RDase) genes were identified. Proteomic workflows identified a putative VC RDase with 49% and 56.1% amino acid similarity to the known VC RDases VcrA and BvcA, respectively. A survey of 1,173 groundwater samples collected from 111 chlorinated solvent-contaminated sites revealed that Dhgm 16S rRNA genes were frequently detected and outnumbered Dhc in 65% of the samples. Dhgm may be more relevant contributors to chlorinated solvent reductive dechlorination in contaminated aquifers than is currently recognized, and non-polluted environments are a source of strictly organohalide-respiring bacteria with novel RDase genes.},
doi = {10.1038/ismej.2017.127},
journal = {The ISME Journal},
number = ,
volume = 11,
place = {United States},
year = {2017},
month = {8}
}

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Works referenced in this record:

Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases
journal, April 2013

  • Hug, Laura A.; Maphosa, Farai; Leys, David
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1616
  • DOI: 10.1098/rstb.2012.0322

STAMP: statistical analysis of taxonomic and functional profiles
journal, July 2014


Aerobic biodegradation of the chloroethenes: pathways, enzymes, ecology, and evolution
journal, July 2010


The Binning of Metagenomic Contigs for Microbial Physiology of Mixed Cultures
journal, January 2012


Harnessing microbial activities for environmental cleanup
journal, June 2006


Noteworthy Facts about a Methane-Producing Microbial Community Processing Acidic Effluent from Sugar Beet Molasses Fermentation
journal, May 2015


"Candidatus Cloacamonas Acidaminovorans": Genome Sequence Reconstruction Provides a First Glimpse of a New Bacterial Division
journal, February 2008

  • Pelletier, E.; Kreimeyer, A.; Bocs, S.
  • Journal of Bacteriology, Vol. 190, Issue 7
  • DOI: 10.1128/JB.01248-07

Dehalogenimonas sp. Strain WBC-2 Genome and Identification of Its trans -Dichloroethene Reductive Dehalogenase, TdrA
journal, October 2015

  • Molenda, Olivia; Quaile, Andrew T.; Edwards, Elizabeth A.
  • Applied and Environmental Microbiology, Vol. 82, Issue 1
  • DOI: 10.1128/AEM.02017-15

Solvent exposures and parkinson disease risk in twins
journal, November 2011

  • Goldman, Samuel M.; Quinlan, Patricia J.; Ross, G. Webster
  • Annals of Neurology, Vol. 71, Issue 6
  • DOI: 10.1002/ana.22629

Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla
journal, September 2012


Essential Histidine and Tryptophan Residues in CcsA, a System II Polytopic Cytochrome c Biogenesis Protein
journal, November 2002

  • Hamel, Patrice P.; Dreyfuss, Beth Welty; Xie, Zhiyi
  • Journal of Biological Chemistry, Vol. 278, Issue 4
  • DOI: 10.1074/jbc.M208651200

Distribution of Organohalide-Respiring Bacteria between Solid and Aqueous Phases
journal, August 2014

  • Cápiro, Natalie L.; Wang, Yonggang; Hatt, Janet K.
  • Environmental Science & Technology, Vol. 48, Issue 18
  • DOI: 10.1021/es501320h

Combined prediction of Tat and Sec signal peptides with hidden Markov models
journal, September 2010


Natural Formation of Vinyl Chloride in the Terrestrial Environment
journal, June 2002

  • Keppler, Frank; Borchers, Reinhard; Pracht, Jens
  • Environmental Science & Technology, Vol. 36, Issue 11
  • DOI: 10.1021/es015611l

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

Novel Major Bacterial Candidate Division within a Municipal Anaerobic Sludge Digester
journal, April 2005


Trichloroethylene and cancer: epidemiologic evidence.
journal, May 2000

  • Wartenberg, D.; Reyner, D.; Scott, C. S.
  • Environmental Health Perspectives, Vol. 108, Issue suppl 2
  • DOI: 10.1289/ehp.00108s2161

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

Phylogenetic and Kinetic Diversity of Aerobic Vinyl Chloride-Assimilating Bacteria from Contaminated Sites
journal, December 2002


Vinyl chloride: still a cause for concern.
journal, July 2000

  • Kielhorn, J.; Melber, C.; Wahnschaffe, U.
  • Environmental Health Perspectives, Vol. 108, Issue 7
  • DOI: 10.1289/ehp.00108579

Quantitative PCR Targeting 16S rRNA and Reductive Dehalogenase Genes Simultaneously Monitors Multiple Dehalococcoides Strains
journal, April 2006


Illuminating Microbial Dark Matter in Meromictic Sakinaw Lake
journal, August 2014

  • Gies, Esther A.; Konwar, Kishori M.; Beatty, J. Thomas
  • Applied and Environmental Microbiology, Vol. 80, Issue 21
  • DOI: 10.1128/AEM.01774-14

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

Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics
journal, December 2010

  • Chourey, Karuna; Jansson, Janet; VerBerkmoes, Nathan
  • Journal of Proteome Research, Vol. 9, Issue 12
  • DOI: 10.1021/pr100787q

Metagenomic Insights into the Evolution, Function, and Complexity of the Planktonic Microbial Community of Lake Lanier, a Temperate Freshwater Ecosystem
journal, July 2011

  • Oh, Seungdae; Caro-Quintero, Alejandro; Tsementzi, Despina
  • Applied and Environmental Microbiology, Vol. 77, Issue 17
  • DOI: 10.1128/AEM.00107-11

Potential Impacts of PCBs on Sediment Microbiomes in a Tropical Marine Environment
journal, February 2016

  • Klaus, James; Kourafalou, Vassiliki; Piggot, Alan
  • Journal of Marine Science and Engineering, Vol. 4, Issue 1
  • DOI: 10.3390/jmse4010013

Formation of chloroacetic acids from soil, humic acid and phenolic moieties
journal, July 2003


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


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


Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductively dehalogenating bacterium isolated from chlorinated solvent-contaminated groundwater
journal, July 2009

  • Moe, W. M.; Yan, J.; Nobre, M. F.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 11
  • DOI: 10.1099/ijs.0.011502-0

Genome sequence of the chlorinated compound–respiring bacterium Dehalococcoides species strain CBDB1
journal, August 2005

  • Kube, Michael; Beck, Alfred; Zinder, Stephen H.
  • Nature Biotechnology, Vol. 23, Issue 10
  • DOI: 10.1038/nbt1131

Genome sequence of the organohalide-respiring Dehalogenimonas alkenigignens type strain (IP3-3T)
journal, June 2016

  • Key, Trent A.; Richmond, Dray P.; Bowman, Kimberly S.
  • Standards in Genomic Sciences, Vol. 11, Issue 1
  • DOI: 10.1186/s40793-016-0165-7

Quantitative PCR Confirms Purity of Strain GT, a Novel Trichloroethene-to-Ethene-Respiring Dehalococcoides Isolate
journal, March 2006


Bacterial dehalorespiration with chlorinated benzenes
journal, November 2000

  • Adrian, Lorenz; Szewzyk, Ulrich; Wecke, Jörg
  • Nature, Vol. 408, Issue 6812
  • DOI: 10.1038/35046063

Dehalococcoides mccartyi Strain DCMB5 Respires a Broad Spectrum of Chlorinated Aromatic Compounds
journal, November 2014

  • Pöritz, Marlén; Schiffmann, Christian L.; Hause, Gerd
  • Applied and Environmental Microbiology, Vol. 81, Issue 2
  • DOI: 10.1128/AEM.02597-14

Genomic characterization of three unique Dehalococcoides that respire on persistent polychlorinated biphenyls
journal, July 2014

  • Wang, S.; Chng, K. R.; Wilm, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 33
  • DOI: 10.1073/pnas.1404845111

Detoxification of vinyl chloride to ethene coupled to growth of an anaerobic bacterium
journal, July 2003

  • He, Jianzhong; Ritalahti, Kirsti M.; Yang, Kun-Lin
  • Nature, Vol. 424, Issue 6944
  • DOI: 10.1038/nature01717

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer
journal, March 2014

  • Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J.
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2013.249

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Biogeochemical and 16S rRNA gene sequence evidence supports a novel mode of anaerobic methanotrophy in permanently ice-covered Lake Fryxell, Antarctica: Methane Oxidation in Lake Fryxell
journal, June 2016

  • Saxton, Matthew A.; Samarkin, Vladimir A.; Schutte, Charles A.
  • Limnology and Oceanography, Vol. 61, Issue S1
  • DOI: 10.1002/lno.10320

Vertical distribution of microbial communities in a perennially stratified Arctic lake with saline, anoxic bottom waters
journal, August 2012

  • Comeau, André M.; Harding, Tommy; Galand, Pierre E.
  • Scientific Reports, Vol. 2, Issue 1
  • DOI: 10.1038/srep00604

Exploring the Correlation between Halorespirer Biomarker Concentrations and TCE Dechlorination Rates
journal, November 2008


Comparative metagenomics of three Dehalococcoides-containing enrichment cultures: the role of the non-dechlorinating community
journal, January 2012


Halocarbons produced by natural oxidation processes during degradation of organic matter
journal, January 2000

  • Keppler, F.; Eiden, R.; Niedan, V.
  • Nature, Vol. 403, Issue 6767
  • DOI: 10.1038/35002055

Relationship between Dehalococcoides DNA in ground water and rates of reductive dechlorination at field scale
journal, September 2006


The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013

  • Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1226

Natural Niche for Organohalide-Respiring Chloroflexi
journal, November 2011

  • Krzmarzick, Mark J.; Crary, Benjamin B.; Harding, Jevon J.
  • Applied and Environmental Microbiology, Vol. 78, Issue 2
  • DOI: 10.1128/AEM.06510-11

Insights into the phylogeny and coding potential of microbial dark matter
journal, July 2013

  • Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12352

Complete genome sequence of Dehalogenimonas lykanthroporepellens type strain (BL-DC-9T) and comparison to “Dehalococcoides” strains
journal, May 2012

  • Siddaramappa, Shivakumara; Challacombe, Jean F.; Delano, Susana F.
  • Standards in Genomic Sciences, Vol. 6, Issue 2
  • DOI: 10.4056/sigs.2806097

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Isolation and characterization of Dehalococcoides sp. strain FL2, a trichloroethene (TCE)- and 1,2-dichloroethene-respiring anaerobe
journal, September 2005


Comparing On-Site to Off-Site Biomass Collection for Dehalococcoides Biomarker Gene Quantification To Predict in Situ Chlorinated Ethene Detoxification Potential
journal, July 2010

  • Ritalahti, Kirsti M.; Hatt, Janet K.; Lugmayr, Veronica
  • Environmental Science & Technology, Vol. 44, Issue 13
  • DOI: 10.1021/es100408r

Bacterial community composition in the water column of the deepest freshwater Lake Baikal as determined by next-generation sequencing
journal, May 2016

  • Kurilkina, Maria I.; Zakharova, Yulia R.; Galachyants, Yuri P.
  • FEMS Microbiology Ecology, Vol. 92, Issue 7
  • DOI: 10.1093/femsec/fiw094

VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data
journal, January 2015


jModelTest 2: more models, new heuristics and parallel computing
journal, July 2012

  • Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón
  • Nature Methods, Vol. 9, Issue 8
  • DOI: 10.1038/nmeth.2109

Detection and Quantification of Dehalogenimonas and "Dehalococcoides" Populations via PCR-Based Protocols Targeting 16S rRNA Genes
journal, October 2009

  • Yan, J.; Rash, B. A.; Rainey, F. A.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23
  • DOI: 10.1128/AEM.01938-09