DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Comparative metagenomics reveals impact of contaminants on groundwater microbiomes

Abstract

To understand patterns of geochemical cycling in pristine versus contaminated groundwater ecosystems, pristine shallow groundwater (FW301) and contaminated groundwater (FW106) samples from the Oak Ridge Integrated Field Research Center (OR-IFRC) were sequenced and compared to each other to determine phylogenetic and metabolic difference between the communities. Proteobacteria (e.g., Burkholderia, Pseudomonas) are the most abundant lineages in the pristine community, though a significant proportion ( > 55%) of the community is composed of poorly characterized low abundance (individually < 1%) lineages. The phylogenetic diversity of the pristine community contributed to a broader diversity of metabolic networks than the contaminated community. In addition, the pristine community encodes redundant and mostly complete geochemical cycles distributed over multiple lineages and appears capable of a wide range of metabolic activities. In contrast, many geochemical cycles in the contaminated community appear truncated or minimized due to decreased biodiversity and dominance by Rhodanobacter populations capable of surviving the combination of stresses at the site. These results indicate that the pristine site contains more robust and encodes more functional redundancy than the stressed community, which contributes to more efficient nutrient cycling and adaptability than the stressed community.

Authors:
 [1];  [2];  [2];  [2];  [3];  [4];  [2];  [2];  [2];  [5];  [6];  [7];  [6];  [8];  [9];  [10];  [11]
  1. Univ. of Oklahoma, Norman, OK (United States); The Univ. of Rhode Island, Kingston, RI (United States)
  2. Univ. of Oklahoma, Norman, OK (United States)
  3. Arizona State Univ., Tempe, AZ (United States)
  4. Univ. of Oklahoma, Norman, OK (United States); Chinese Academy of Sciences (CAS), Beijing (China)
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Montana State Univ., Bozeman, MT (United States)
  8. Michigan State Univ., East Lansing, MI (United States)
  9. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  10. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  11. Univ. of Oklahoma, Norman, OK (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Tsinghua Univ., Beijing (China)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1327637
Alternate Identifier(s):
OSTI ID: 1255538; OSTI ID: 1407297
Grant/Contract Number:  
AC05-00OR22725; FG02-07ER64398; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; metagenomics; bioremediation; groundwater microbiology

Citation Formats

Hemme, Christopher L., Tu, Qichao, Shi, Zhou, Qin, Yujia, Gao, Weimin, Deng, Ye, Nostrand, Joy D. Van, Wu, Liyou, He, Zhili, Chain, Patrick S. G., Tringe, Susannah G., Fields, Matthew W., Rubin, Edward M., Tiedje, James M., Hazen, Terry C., Arkin, Adam P., and Zhou, Jizhong. Comparative metagenomics reveals impact of contaminants on groundwater microbiomes. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.01205.
Hemme, Christopher L., Tu, Qichao, Shi, Zhou, Qin, Yujia, Gao, Weimin, Deng, Ye, Nostrand, Joy D. Van, Wu, Liyou, He, Zhili, Chain, Patrick S. G., Tringe, Susannah G., Fields, Matthew W., Rubin, Edward M., Tiedje, James M., Hazen, Terry C., Arkin, Adam P., & Zhou, Jizhong. Comparative metagenomics reveals impact of contaminants on groundwater microbiomes. United States. https://doi.org/10.3389/fmicb.2015.01205
Hemme, Christopher L., Tu, Qichao, Shi, Zhou, Qin, Yujia, Gao, Weimin, Deng, Ye, Nostrand, Joy D. Van, Wu, Liyou, He, Zhili, Chain, Patrick S. G., Tringe, Susannah G., Fields, Matthew W., Rubin, Edward M., Tiedje, James M., Hazen, Terry C., Arkin, Adam P., and Zhou, Jizhong. Sat . "Comparative metagenomics reveals impact of contaminants on groundwater microbiomes". United States. https://doi.org/10.3389/fmicb.2015.01205. https://www.osti.gov/servlets/purl/1327637.
@article{osti_1327637,
title = {Comparative metagenomics reveals impact of contaminants on groundwater microbiomes},
author = {Hemme, Christopher L. and Tu, Qichao and Shi, Zhou and Qin, Yujia and Gao, Weimin and Deng, Ye and Nostrand, Joy D. Van and Wu, Liyou and He, Zhili and Chain, Patrick S. G. and Tringe, Susannah G. and Fields, Matthew W. and Rubin, Edward M. and Tiedje, James M. and Hazen, Terry C. and Arkin, Adam P. and Zhou, Jizhong},
abstractNote = {To understand patterns of geochemical cycling in pristine versus contaminated groundwater ecosystems, pristine shallow groundwater (FW301) and contaminated groundwater (FW106) samples from the Oak Ridge Integrated Field Research Center (OR-IFRC) were sequenced and compared to each other to determine phylogenetic and metabolic difference between the communities. Proteobacteria (e.g., Burkholderia, Pseudomonas) are the most abundant lineages in the pristine community, though a significant proportion ( > 55%) of the community is composed of poorly characterized low abundance (individually < 1%) lineages. The phylogenetic diversity of the pristine community contributed to a broader diversity of metabolic networks than the contaminated community. In addition, the pristine community encodes redundant and mostly complete geochemical cycles distributed over multiple lineages and appears capable of a wide range of metabolic activities. In contrast, many geochemical cycles in the contaminated community appear truncated or minimized due to decreased biodiversity and dominance by Rhodanobacter populations capable of surviving the combination of stresses at the site. These results indicate that the pristine site contains more robust and encodes more functional redundancy than the stressed community, which contributes to more efficient nutrient cycling and adaptability than the stressed community.},
doi = {10.3389/fmicb.2015.01205},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Sat Oct 31 00:00:00 EDT 2015},
month = {Sat Oct 31 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 52 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


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

Millimeter‐scale genetic gradients and community‐level molecular convergence in a hypersaline microbial mat
journal, January 2008

  • Kunin, Victor; Raes, Jeroen; Harris, J. Kirk
  • Molecular Systems Biology, Vol. 4, Issue 1
  • DOI: 10.1038/msb.2008.35

Comparative Metagenomics of Microbial Communities
journal, April 2005


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

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

Strategies for Enhancing the Effectiveness of Metagenomic-based Enzyme Discovery in Lignocellulolytic Microbial Communities
journal, March 2010

  • DeAngelis, Kristen M.; Gladden, John M.; Allgaier, Martin
  • BioEnergy Research, Vol. 3, Issue 2
  • DOI: 10.1007/s12155-010-9089-z

CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


The integrated microbial genomes system: an expanding comparative analysis resource
journal, October 2009

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp887

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Phylogenetic and Functional Biomakers as Indicators of Bacterial Community Responses to Mixed-Waste Contamination
journal, April 2006

  • Fields, M. W.; Bagwell, C. E.; Carroll, S. L.
  • Environmental Science & Technology, Vol. 40, Issue 8
  • DOI: 10.1021/es051748q

Dynamics of Microbial Community Composition and Function during In Situ Bioremediation of a Uranium-Contaminated Aquifer
journal, April 2011

  • Van Nostrand, Joy D.; Wu, Liyou; Wu, Wei-Min
  • Applied and Environmental Microbiology, Vol. 77, Issue 11
  • DOI: 10.1128/AEM.01981-10

Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community
journal, February 2010

  • Hemme, Christopher L.; Deng, Ye; Gentry, Terry J.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.154

Mineralogical characterization of saprolite at the FRC background site in Oak Ridge, Tennessee
journal, December 2008


Horizontal Gene Transfer of PIB-Type ATPases among Bacteria Isolated from Radionuclide- and Metal-Contaminated Subsurface Soils
journal, May 2006


IMG/M: a data management and analysis system for metagenomes
journal, December 2007

  • Markowitz, V. M.; Ivanova, N. N.; Szeto, E.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm869

Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments
journal, December 1988


Global modeling of withdrawal, allocation and consumptive use of surface water and groundwater resources
journal, January 2014

  • Wada, Y.; Wisser, D.; Bierkens, M. F. P.
  • Earth System Dynamics, Vol. 5, Issue 1
  • DOI: 10.5194/esd-5-15-2014

GeoChip-based analysis of functional microbial communities during the reoxidation of a bioreduced uranium-contaminated aquifer
journal, October 2009


Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure
journal, August 2008

  • Moreels, David; Crosson, Garry; Garafola, Craig
  • Environmental Science and Pollution Research, Vol. 15, Issue 6
  • DOI: 10.1007/s11356-008-0034-z

Potential for In Situ Bioremediation of a Low-pH, High-Nitrate Uranium-Contaminated Groundwater
journal, November 2003

  • Shelobolina, Evgenya S.; O'Neill, Kathleen; Finneran, Kevin T.
  • Soil and Sediment Contamination: An International Journal, Vol. 12, Issue 6
  • DOI: 10.1080/714037720

Short read fragment assembly of bacterial genomes
journal, February 2008

  • Chaisson, M. J.; Pevzner, P. A.
  • Genome Research, Vol. 18, Issue 2
  • DOI: 10.1101/gr.7088808

Change in Bacterial Community Structure during In Situ Biostimulation of Subsurface Sediment Cocontaminated with Uranium and Nitrate
journal, August 2004


Metagenomic comparison of microbial communities inhabiting confined and unconfined aquifer ecosystems: Aquifer metagenomics
journal, October 2011


Hydrologic Significance of Carbon Monoxide Concentrations in Ground Water
journal, May 2007


Community structure and metabolism through reconstruction of microbial genomes from the environment
journal, February 2004

  • Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip
  • Nature, Vol. 428, Issue 6978
  • DOI: 10.1038/nature02340

Molecular Evidence for the Evolution of Metal Homeostasis Genes by Lateral Gene Transfer in Bacteria from the Deep Terrestrial Subsurface
journal, March 2004


Using Hydrochemical Fades to Delineate Ground Water Flowpaths in Fractured Shale
journal, February 1999


Groundwater: the processes and global significance of aquifer degradation
journal, November 2003

  • Foster, S. S. D.; Chilton, P. J.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 358, Issue 1440
  • DOI: 10.1098/rstb.2003.1380

Scaffolding pre-assembled contigs using SSPACE
journal, December 2010


The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes
journal, September 2008


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

Microbial Communities in Contaminated Sediments, Associated with Bioremediation of Uranium to Submicromolar Levels
journal, May 2008

  • Cardenas, E.; Wu, W. -M.; Leigh, M. B.
  • Applied and Environmental Microbiology, Vol. 74, Issue 12
  • DOI: 10.1128/AEM.02308-07

IMG ER: a system for microbial genome annotation expert review and curation
journal, June 2009


Identifying biologically relevant differences between metagenomic communities
journal, February 2010


High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton
journal, June 2011

  • Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J.
  • The ISME Journal, Vol. 6, Issue 1
  • DOI: 10.1038/ismej.2011.84

Mineralogical characterization of saprolite at the FRC background site in Oak Ridge, Tennessee
journal, December 2008


Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure
journal, August 2008

  • Moreels, David; Crosson, Garry; Garafola, Craig
  • Environmental Science and Pollution Research, Vol. 15, Issue 6
  • DOI: 10.1007/s11356-008-0034-z

Strategies for Enhancing the Effectiveness of Metagenomic-based Enzyme Discovery in Lignocellulolytic Microbial Communities
journal, March 2010

  • DeAngelis, Kristen M.; Gladden, John M.; Allgaier, Martin
  • BioEnergy Research, Vol. 3, Issue 2
  • DOI: 10.1007/s12155-010-9089-z

Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments
journal, December 1988


Phylogenetic and Functional Biomakers as Indicators of Bacterial Community Responses to Mixed-Waste Contamination
journal, April 2006

  • Fields, M. W.; Bagwell, C. E.; Carroll, S. L.
  • Environmental Science & Technology, Vol. 40, Issue 8
  • DOI: 10.1021/es051748q

Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community
journal, February 2010

  • Hemme, Christopher L.; Deng, Ye; Gentry, Terry J.
  • The ISME Journal, Vol. 4, Issue 5
  • DOI: 10.1038/ismej.2009.154

High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton
journal, June 2011

  • Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J.
  • The ISME Journal, Vol. 6, Issue 1
  • DOI: 10.1038/ismej.2011.84

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

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

Millimeter‐scale genetic gradients and community‐level molecular convergence in a hypersaline microbial mat
journal, January 2008

  • Kunin, Victor; Raes, Jeroen; Harris, J. Kirk
  • Molecular Systems Biology, Vol. 4, Issue 1
  • DOI: 10.1038/msb.2008.35

Horizontal gene transfer enables programmable gene stability in synthetic microbiota
journal, September 2022


Potential for In Situ Bioremediation of a Low-pH, High-Nitrate Uranium-Contaminated Groundwater
journal, November 2003

  • Shelobolina, Evgenya S.; O'Neill, Kathleen; Finneran, Kevin T.
  • Soil and Sediment Contamination: An International Journal, Vol. 12, Issue 6
  • DOI: 10.1080/714037720

Identifying biologically relevant differences between metagenomic communities
journal, February 2010


Scaffolding pre-assembled contigs using SSPACE
journal, December 2010


UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


IMG/M: a data management and analysis system for metagenomes
journal, December 2007

  • Markowitz, V. M.; Ivanova, N. N.; Szeto, E.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm869

The integrated microbial genomes system: an expanding comparative analysis resource
journal, October 2009

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 38, Issue suppl_1
  • DOI: 10.1093/nar/gkp887

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Short read fragment assembly of bacterial genomes
journal, February 2008

  • Chaisson, M. J.; Pevzner, P. A.
  • Genome Research, Vol. 18, Issue 2
  • DOI: 10.1101/gr.7088808

GeoChip-based analysis of functional microbial communities during the reoxidation of a bioreduced uranium-contaminated aquifer
journal, October 2009


Hydrologic Significance of Carbon Monoxide Concentrations in Ground Water
journal, May 2007


Using Hydrochemical Fades to Delineate Ground Water Flowpaths in Fractured Shale
journal, February 1999


Comparative Metagenomics of Microbial Communities
journal, April 2005


DNA recovery from soils of diverse composition.
journal, January 1996


The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes
journal, September 2008


Works referencing / citing this record:

The bacterial community structure and functional profile in the heavy metal contaminated paddy soils, surrounding a nonferrous smelter in South Korea
journal, May 2018

  • Tipayno, Sherlyn C.; Truu, Jaak; Samaddar, Sandipan
  • Ecology and Evolution, Vol. 8, Issue 12
  • DOI: 10.1002/ece3.4170

Metagenomic applications in environmental monitoring and bioremediation
journal, August 2016

  • Techtmann, Stephen M.; Hazen, Terry C.
  • Journal of Industrial Microbiology & Biotechnology, Vol. 43, Issue 10
  • DOI: 10.1007/s10295-016-1809-8

The selective pressures on the microbial community in a metal-contaminated aquifer
journal, December 2018


A marine plasmid hitchhiking vast phylogenetic and geographic distances
journal, September 2019

  • Petersen, Jörn; Vollmers, John; Ringel, Victoria
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 41
  • DOI: 10.1073/pnas.1905878116

Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments
journal, September 2018

  • Smith, H. J.; Zelaya, A. J.; De León, K. B.
  • FEMS Microbiology Ecology, Vol. 94, Issue 12
  • DOI: 10.1093/femsec/fiy191

Dimethyl phthalate altered the microbial metabolic pathways in a Mollisol: Environmental behaviour of dimethyl phthalate in soil
journal, March 2018

  • Wang, Z. G.; You, Y. M.; Xu, W. H.
  • European Journal of Soil Science, Vol. 69, Issue 3
  • DOI: 10.1111/ejss.12545

Analysis and correction of compositional bias in sparse sequencing count data
journal, November 2018


Comprehensive benchmarking and ensemble approaches for metagenomic classifiers
journal, September 2017


Evaluation of Lysis Methods for the Extraction of Bacterial DNA for Analysis of the Vaginal Microbiota
journal, September 2016


Pseudomonas aeruginosa displays a dormancy phenotype during long-term survival in water
journal, September 2018


Metagenomic Evaluation of Bacterial and Fungal Assemblages Enriched within Diffusion Chambers and Microbial Traps Containing Uraniferous Soils
journal, September 2019


Physiological Profiling and Functional Diversity of Groundwater Microbial Communities in a Municipal Solid Waste Landfill Area
journal, December 2019

  • Melita, Marco; Amalfitano, Stefano; Preziosi, Elisabetta
  • Water, Vol. 11, Issue 12
  • DOI: 10.3390/w11122624

A marine plasmid hitchhiking vast phylogenetic and geographic distances
text, January 2019


Comprehensive Benchmarking and Ensemble Approaches for Metagenomic Classifiers
journal, June 2017

  • McIntyre, Alexa B. R.; Ounit, Rachid; Afshinnekoo, Ebrahim
  • Genome Biology
  • DOI: 10.1101/156919

Analysis and correction of compositional bias in sparse sequencing count data
posted_content, January 2018

  • Kumar, M. Senthil; Slud, Eric V.; Okrah, Kwame
  • BMC Genomics
  • DOI: 10.1101/142851

The selective pressures on the microbial community in a metal-contaminated aquifer
journal, December 2018


Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments
journal, September 2018

  • Smith, H. J.; Zelaya, A. J.; De León, K. B.
  • FEMS Microbiology Ecology, Vol. 94, Issue 12
  • DOI: 10.1093/femsec/fiy191

Correction to: Comprehensive benchmarking and ensemble approaches for metagenomic classifiers
journal, April 2019


Evaluation of Lysis Methods for the Extraction of Bacterial DNA for Analysis of the Vaginal Microbiota
journal, September 2016


A marine plasmid hitchhiking vast phylogenetic and geographic distances
text, January 2019