Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation
Abstract
Temporal variability complicates testing the influences of environmental variability on microbial community structure and thus function. An in-field bioreactor system was developed to assess oxic versus anoxic manipulations on in situ groundwater communities. Each sample was sequenced (16S SSU rRNA genes, average 10,000 reads), and biogeochemical parameters are monitored by quantifying 53 metals, 12 organic acids, 14 anions, and 3 sugars. Changes in dissolved oxygen (DO), pH, and other variables were similar across bioreactors. Sequencing revealed a complex community that fluctuated in-step with the groundwater community and responded to DO. This also directly influenced the pH, and so the biotic impacts of DO and pH shifts are correlated. A null model demonstrated that bioreactor communities were driven in part not only by experimental conditions but also by stochastic variability and did not accurately capture alterations in diversity during perturbations. We identified two groups of abundant OTUs important to this system; one was abundant in high DO and pH and contained heterotrophs and oxidizers of iron, nitrite, and ammonium, whereas the other was abundant in low DO with the capability to reduce nitrate. In-field bioreactors are a powerful tool for capturing natural microbial community responses to alterations in geochemical factors beyondmore »
- Authors:
-
more »
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Johns Hopkins Univ., Baltimore, MD (United States)
- Colorado State Univ., Fort Collins, CO (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Oklahoma, Norman, OK (United States)
- Univ. of Georgia, Athens, GA (United States)
- Montana State Univ., Bozeman, MT (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- 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:
- 1348330
- Alternate Identifier(s):
- OSTI ID: 1476466
- Grant/Contract Number:
- AC05-00OR22725; AC02-05CH11231
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Environmental Science and Technology
- Additional Journal Information:
- Journal Volume: 51; Journal Issue: 5; Journal ID: ISSN 0013-936X
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Bioreactor; Microbial Community; Groundwater
Citation Formats
King, Andrew J., Preheim, Sarah P., Bailey, Kathryn L., Robeson, Michael S., Roy Chowdhury, Taniya, Crable, Bryan R., Hurt, Richard A., Mehlhorn, Tonia, Lowe, Kenneth A., Phelps, Tommy J., Palumbo, Anthony V., Brandt, Craig C., Brown, Steven D., Podar, Mircea, Zhang, Ping, Lancaster, W. Andrew, Poole, Farris, Watson, David B., W. Fields, Matthew, Chandonia, John-Marc, Alm, Eric J., Zhou, Jizhong, Adams, Michael W. W., Hazen, Terry C., Arkin, Adam P., and Elias, Dwayne A. Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation. United States: N. p., 2017.
Web. doi:10.1021/acs.est.6b04751.
King, Andrew J., Preheim, Sarah P., Bailey, Kathryn L., Robeson, Michael S., Roy Chowdhury, Taniya, Crable, Bryan R., Hurt, Richard A., Mehlhorn, Tonia, Lowe, Kenneth A., Phelps, Tommy J., Palumbo, Anthony V., Brandt, Craig C., Brown, Steven D., Podar, Mircea, Zhang, Ping, Lancaster, W. Andrew, Poole, Farris, Watson, David B., W. Fields, Matthew, Chandonia, John-Marc, Alm, Eric J., Zhou, Jizhong, Adams, Michael W. W., Hazen, Terry C., Arkin, Adam P., & Elias, Dwayne A. Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation. United States. https://doi.org/10.1021/acs.est.6b04751
King, Andrew J., Preheim, Sarah P., Bailey, Kathryn L., Robeson, Michael S., Roy Chowdhury, Taniya, Crable, Bryan R., Hurt, Richard A., Mehlhorn, Tonia, Lowe, Kenneth A., Phelps, Tommy J., Palumbo, Anthony V., Brandt, Craig C., Brown, Steven D., Podar, Mircea, Zhang, Ping, Lancaster, W. Andrew, Poole, Farris, Watson, David B., W. Fields, Matthew, Chandonia, John-Marc, Alm, Eric J., Zhou, Jizhong, Adams, Michael W. W., Hazen, Terry C., Arkin, Adam P., and Elias, Dwayne A. 2017.
"Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation". United States. https://doi.org/10.1021/acs.est.6b04751. https://www.osti.gov/servlets/purl/1348330.
@article{osti_1348330,
title = {Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation},
author = {King, Andrew J. and Preheim, Sarah P. and Bailey, Kathryn L. and Robeson, Michael S. and Roy Chowdhury, Taniya and Crable, Bryan R. and Hurt, Richard A. and Mehlhorn, Tonia and Lowe, Kenneth A. and Phelps, Tommy J. and Palumbo, Anthony V. and Brandt, Craig C. and Brown, Steven D. and Podar, Mircea and Zhang, Ping and Lancaster, W. Andrew and Poole, Farris and Watson, David B. and W. Fields, Matthew and Chandonia, John-Marc and Alm, Eric J. and Zhou, Jizhong and Adams, Michael W. W. and Hazen, Terry C. and Arkin, Adam P. and Elias, Dwayne A.},
abstractNote = {Temporal variability complicates testing the influences of environmental variability on microbial community structure and thus function. An in-field bioreactor system was developed to assess oxic versus anoxic manipulations on in situ groundwater communities. Each sample was sequenced (16S SSU rRNA genes, average 10,000 reads), and biogeochemical parameters are monitored by quantifying 53 metals, 12 organic acids, 14 anions, and 3 sugars. Changes in dissolved oxygen (DO), pH, and other variables were similar across bioreactors. Sequencing revealed a complex community that fluctuated in-step with the groundwater community and responded to DO. This also directly influenced the pH, and so the biotic impacts of DO and pH shifts are correlated. A null model demonstrated that bioreactor communities were driven in part not only by experimental conditions but also by stochastic variability and did not accurately capture alterations in diversity during perturbations. We identified two groups of abundant OTUs important to this system; one was abundant in high DO and pH and contained heterotrophs and oxidizers of iron, nitrite, and ammonium, whereas the other was abundant in low DO with the capability to reduce nitrate. In-field bioreactors are a powerful tool for capturing natural microbial community responses to alterations in geochemical factors beyond the bulk phase.},
doi = {10.1021/acs.est.6b04751},
url = {https://www.osti.gov/biblio/1348330},
journal = {Environmental Science and Technology},
issn = {0013-936X},
number = 5,
volume = 51,
place = {United States},
year = {Mon Jan 23 00:00:00 EST 2017},
month = {Mon Jan 23 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
A Limited Microbial Consortium Is Responsible for Extended Bioreduction of Uranium in a Contaminated Aquifer
journal, July 2011
- Gihring, Thomas M.; Zhang, Gengxin; Brandt, Craig C.
- Applied and Environmental Microbiology, Vol. 77, Issue 17
A new method for non-parametric multivariate analysis of variance
journal, February 2001
- Anderson, Marti J.
- Austral Ecology, Vol. 26, Issue 1
National survey of molecular bacterial diversity of New Zealand groundwater: relationships between biodiversity, groundwater chemistry and aquifer characteristics
journal, August 2013
- Sirisena, Kosala A.; Daughney, Christopher J.; Moreau-Fournier, Magali
- FEMS Microbiology Ecology, Vol. 86, Issue 3
DNA recovery from soils of diverse composition.
journal, January 1996
- Zhou, J.; Bruns, M. A.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 62, Issue 2
Stoichiometry and temperature sensitivity of methanogenesis and CO 2 production from saturated polygonal tundra in Barrow, Alaska
journal, November 2014
- Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J.
- Global Change Biology, Vol. 21, Issue 2
Monitoring impact of in situ biostimulation treatment on groundwater bacterial community by DGGE
journal, April 2000
- Iwamoto, Tomotada; Tani, Katsuji; Nakamura, Kanji
- FEMS Microbiology Ecology, Vol. 32, Issue 2
Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths
journal, September 2008
- Hwang, Chiachi; Wu, Weimin; Gentry, Terry J.
- The ISME Journal, Vol. 3, Issue 1
Decreases in average bacterial community rRNA operon copy number during succession
journal, November 2015
- Nemergut, Diana R.; Knelman, Joseph E.; Ferrenberg, Scott
- The ISME Journal, Vol. 10, Issue 5
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007
- He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
- The ISME Journal, Vol. 1, Issue 1
Biopython: freely available Python tools for computational molecular biology and bioinformatics
journal, March 2009
- Cock, P. J. A.; Antao, T.; Chang, J. T.
- Bioinformatics, Vol. 25, Issue 11
Source specific fecal bacteria modeling using soil and water assessment tool model
journal, January 2009
- Parajuli, Prem B.; Mankin, Kyle R.; Barnes, Philip L.
- Bioresource Technology, Vol. 100, Issue 2
Application of a High-Density Oligonucleotide Microarray Approach To Study Bacterial Population Dynamics during Uranium Reduction and Reoxidation
journal, September 2006
- Brodie, E. L.; DeSantis, T. Z.; Joyner, D. C.
- Applied and Environmental Microbiology, Vol. 72, Issue 9
Microbial communities in karst groundwater and their potential use for biomonitoring
journal, August 2008
- Pronk, Michiel; Goldscheider, Nico; Zopfi, Jakob
- Hydrogeology Journal, Vol. 17, Issue 1
Spatial and temporal changes in microbial community structure associated with recharge-influenced chemical gradients in a contaminated aquifer
journal, May 2004
- Haack, Sheridan K.; Fogarty, Lisa R.; West, Toby G.
- Environmental Microbiology, Vol. 6, Issue 5
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
Perspectives and predictions on the microbial ecology of the hyporheic zone
journal, February 1999
- Storey, R. G.; Fulthorpe, R. R.; Williams, D. D.
- Freshwater Biology, Vol. 41, Issue 1
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Environmental Whole-Genome Amplification To Access Microbial Populations in Contaminated Sediments
journal, May 2006
- Abulencia, C. B.; Wyborski, D. L.; Garcia, J. A.
- Applied and Environmental Microbiology, Vol. 72, Issue 5
Inferring Correlation Networks from Genomic Survey Data
journal, September 2012
- Friedman, Jonathan; Alm, Eric J.
- PLoS Computational Biology, Vol. 8, Issue 9
Changes in bacterial community structure correlate with initial operating conditions of a field-scale denitrifying fluidized bed reactor
journal, November 2005
- Hwang, C.; Wu, W. -M.; Gentry, T. J.
- Applied Microbiology and Biotechnology, Vol. 71, Issue 5
Spatial and temporal small-scale variation in groundwater quality of a shallow sandy aquifer
journal, February 1992
- Bjerg, Poul L.; Christensen, Thomas H.
- Journal of Hydrology, Vol. 131, Issue 1-4
Metallomics of two microorganisms relevant to heavy metal bioremediation reveal fundamental differences in metal assimilation and utilization
journal, January 2014
- Lancaster, W. Andrew; Menon, Angeli Lal; Scott, Israel
- Metallomics, Vol. 6, Issue 5
Spatio-temporal patterns of microbial communities in a hydrologically dynamic pristine aquifer
journal, April 2012
- Zhou, Yuxiang; Kellermann, Claudia; Griebler, Christian
- FEMS Microbiology Ecology, Vol. 81, Issue 1
Hexavalent Chromium Reduction under Fermentative Conditions with Lactate Stimulated Native Microbial Communities
journal, December 2013
- Somenahally, Anil C.; Mosher, Jennifer J.; Yuan, Tong
- PLoS ONE, Vol. 8, Issue 12
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
Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis
journal, June 2015
- Wu, Liyou; Wen, Chongqing; Qin, Yujia
- BMC Microbiology, Vol. 15, Issue 1
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
Hierarchical Grouping to Optimize an Objective Function
journal, March 1963
- Ward, Joe H.
- Journal of the American Statistical Association, Vol. 58, Issue 301
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters
journal, April 2014
- Vanwonterghem, Inka; Jensen, Paul D.; Dennis, Paul G.
- The ISME Journal, Vol. 8, Issue 10
Non-parametric multivariate analyses of changes in community structure
journal, March 1993
- Clarke, K. R.
- Austral Ecology, Vol. 18, Issue 1
Disturbance in Marine Intertidal Boulder Fields: The Nonequilibrium Maintenance of Species Diversity
journal, December 1979
- Sousa, Wayne P.
- Ecology, Vol. 60, Issue 6
Ecology and management of the hyporheic zone: stream–groundwater interactions of running waters and their floodplains
journal, March 2010
- Boulton, Andrew J.; Datry, Thibault; Kasahara, Tamao
- Journal of the North American Benthological Society, Vol. 29, Issue 1
Microbial Community Succession during Lactate Amendment and Electron Acceptor Limitation Reveals a Predominance of Metal-Reducing Pelosinus spp.
journal, January 2012
- Mosher, Jennifer J.; Phelps, Tommy J.; Podar, Mircea
- Applied and Environmental Microbiology, Vol. 78, Issue 7
Change in Bacterial Community Structure during In Situ Biostimulation of Subsurface Sediment Cocontaminated with Uranium and Nitrate
journal, August 2004
- North, N. N.; Dollhopf, S. L.; Petrie, L.
- Applied and Environmental Microbiology, Vol. 70, Issue 8
A high-resolution non-invasive approach to quantify oxygen transport across the capillary fringe and within the underlying groundwater
journal, March 2011
- Haberer, Christina M.; Rolle, Massimo; Liu, Sanheng
- Journal of Contaminant Hydrology, Vol. 122, Issue 1-4
Influence of depth and time on diversity of free-living microbial community in the variably saturated zone of a granitic aquifer
journal, January 2012
- Bougon, Nolwenn; Aquilina, Luc; Molénat, Jérome
- FEMS Microbiology Ecology, Vol. 80, Issue 1
Microbial biodiversity in groundwater ecosystems
journal, April 2009
- Griebler, C.; Lueders, T.
- Freshwater Biology, Vol. 54, Issue 4
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Significant Association between Sulfate-Reducing Bacteria and Uranium-Reducing Microbial Communities as Revealed by a Combined Massively Parallel Sequencing-Indicator Species Approach
journal, August 2010
- Cardenas, E.; Wu, W. -M.; Leigh, M. B.
- Applied and Environmental Microbiology, Vol. 76, Issue 20
Spatial and Temporal Variation in Groundwater Nitrate Removal in a Riparian Forest
journal, July 1995
- Nelson, William M.; Gold, Arthur J.; Groffman, Peter M.
- Journal of Environmental Quality, Vol. 24, Issue 4
Impacts of inundation and drought on eukaryote biodiversity in semi-arid floodplain soils
journal, February 2013
- Baldwin, Darren S.; Colloff, Matthew J.; Rees, Gavin N.
- Molecular Ecology, Vol. 22, Issue 6
Microbial Community Responses to Organophosphate Substrate Additions in Contaminated Subsurface Sediments
journal, June 2014
- Martinez, Robert J.; Wu, Cindy H.; Beazley, Melanie J.
- PLoS ONE, Vol. 9, Issue 6
The significance of microbial processes in hydrogeology and geochemistry
journal, March 2000
- Chapelle, Francis H.
- Hydrogeology Journal, Vol. 8, Issue 1
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Defining seasonal marine microbial community dynamics
journal, August 2011
- Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory
- The ISME Journal, Vol. 6, Issue 2
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
Habitat Heterogeneity and Associated Microbial Community Structure in a Small-Scale Floodplain Hyporheic Flow Path
journal, May 2009
- Lowell, Jennifer L.; Gordon, Nathan; Engstrom, Dale
- Microbial Ecology, Vol. 58, Issue 3
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005
- Lozupone, C.; Knight, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Geochemistry of a Permeable Reactive Barrier for Metals and Acid Mine Drainage
journal, August 1999
- Benner, S. G.; Blowes, D. W.; Gould, W. D.
- Environmental Science & Technology, Vol. 33, Issue 16
Predicting bacterial community assemblages using an artificial neural network approach
journal, April 2012
- Larsen, Peter E.; Field, Dawn; Gilbert, Jack A.
- Nature Methods, Vol. 9, Issue 6
Functional Diversity and Electron Donor Dependence of Microbial Populations Capable of U(VI) Reduction in Radionuclide-Contaminated Subsurface Sediments
journal, March 2008
- Akob, D. M.; Mills, H. J.; Gihring, T. M.
- Applied and Environmental Microbiology, Vol. 74, Issue 10
Spatial and temporal patterns of bacterial density and metabolic activity in a karst aquifer [Spatial and temporal patterns of bacterial density and metabolic activity in a karst aquifer]
journal, March 2001
- Simon, K. S.; Gibert, J.; Petitot, P.
- Fundamental and Applied Limnology, Vol. 151, Issue 1
The microbial ocean from genomes to biomes
journal, May 2009
- DeLong, Edward F.
- Nature, Vol. 459, Issue 7244
Toward an Ecological Classification of soil Bacteria
journal, June 2007
- Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
- Ecology, Vol. 88, Issue 6
Works referencing / citing this record:
Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
journal, February 2019
- Kothari, Ankita; Wu, Yu-Wei; Chandonia, John-Marc
- mBio, Vol. 10, Issue 1
Use of in-field bioreactors demonstrate groundwater filtration influences planktonic bacterial community assembly, but not biofilm composition
journal, March 2018
- Christensen, Geoff A.; Moon, JiWon; Veach, Allison M.
- PLOS ONE, Vol. 13, Issue 3
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
Large Circular Plasmids from Groundwater Plasmidomes Span Multiple Incompatibility Groups and Are Enriched in Multimetal Resistance Genes
journal, February 2019
- Kothari, Ankita; Wu, Yu-Wei; Chandonia, John-Marc
- mBio, Vol. 10, Issue 1
Use of in-field bioreactors demonstrate groundwater filtration influences planktonic bacterial community assembly, but not biofilm composition
journal, March 2018
- Christensen, Geoff A.; Moon, JiWon; Veach, Allison M.
- PLOS ONE, Vol. 13, Issue 3