In-field bioreactors demonstrate dynamic shifts in microbial communities in response to geochemical perturbations
Abstract
Subsurface microbial communities mediate the transformation and fate of redox sensitive materials including organic matter, metals and radionuclides. Few studies have explored how changing geochemical conditions influence the composition of groundwater microbial communities over time. We temporally monitored alterations in abiotic forces on microbial community structure using 1L in-field bioreactors receiving background and contaminated groundwater at the Oak Ridge Reservation, TN. Planktonic and biofilm microbial communities were initialized with background water for 4 days to establish communities in triplicate control reactors and triplicate test reactors and then fed filtered water for 14 days. On day 18, three reactors were switched to receive filtered groundwater from a contaminated well, enriched in total dissolved solids relative to the background site, particularly chloride, nitrate, uranium, and sulfate. Biological and geochemical data were collected throughout the experiment, including planktonic and biofilm DNA for 16S rRNA amplicon sequencing, cell counts, total protein, anions, cations, trace metals, organic acids, bicarbonate, pH, Eh, DO, and conductivity. We observed significant shifts in both planktonic and biofilm microbial communities receiving contaminated water. This included a loss of rare taxa, especially amongst members of the Bacteroidetes, Acidobacteria, Chloroflexi, and Betaproteobacteria, but enrichment in the Fe- and nitrate- reducing Ferribacterium andmore »
- Authors:
-
[1];
[1];
[3];
[5];
[9];
[1]
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); US Geological Survey, Reston, VA (United States)
- Univ. of Tennessee, Knoxville, TN (United States)
- Montana State Univ., Bozeman, MT (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Univ. of Georgia, Athens, GA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of Oklahoma, Norman, OK (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (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:
- 1671429
- Alternate Identifier(s):
- OSTI ID: 1713221
- Grant/Contract Number:
- AC05-00OR22725; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 9; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; water pollution; geochemistry; sediment; biofilms; community structure; nitrates; contaminants; bacterial biofilms
Citation Formats
Wilpiszeski, Regina L., Gionfriddo, Caitlin M., Wymore, Ann M., Moon, Ji-Won, Lowe, Kenneth A., Podar, Mircea, Rafie, Sa’ad, Fields, Matthew W., Hazen, Terry C., Ge, Xiaoxuan, Poole, Farris, Adams, Michael W., Chakraborty, Romy, Fan, Yupeng, Van Nostrand, Joy D., Zhou, Jizhong, Arkin, Adam P., and Elias, Dwayne A. In-field bioreactors demonstrate dynamic shifts in microbial communities in response to geochemical perturbations. United States: N. p., 2020.
Web. doi:10.1371/journal.pone.0232437.
Wilpiszeski, Regina L., Gionfriddo, Caitlin M., Wymore, Ann M., Moon, Ji-Won, Lowe, Kenneth A., Podar, Mircea, Rafie, Sa’ad, Fields, Matthew W., Hazen, Terry C., Ge, Xiaoxuan, Poole, Farris, Adams, Michael W., Chakraborty, Romy, Fan, Yupeng, Van Nostrand, Joy D., Zhou, Jizhong, Arkin, Adam P., & Elias, Dwayne A. In-field bioreactors demonstrate dynamic shifts in microbial communities in response to geochemical perturbations. United States. https://doi.org/10.1371/journal.pone.0232437
Wilpiszeski, Regina L., Gionfriddo, Caitlin M., Wymore, Ann M., Moon, Ji-Won, Lowe, Kenneth A., Podar, Mircea, Rafie, Sa’ad, Fields, Matthew W., Hazen, Terry C., Ge, Xiaoxuan, Poole, Farris, Adams, Michael W., Chakraborty, Romy, Fan, Yupeng, Van Nostrand, Joy D., Zhou, Jizhong, Arkin, Adam P., and Elias, Dwayne A. Mon .
"In-field bioreactors demonstrate dynamic shifts in microbial communities in response to geochemical perturbations". United States. https://doi.org/10.1371/journal.pone.0232437. https://www.osti.gov/servlets/purl/1671429.
@article{osti_1671429,
title = {In-field bioreactors demonstrate dynamic shifts in microbial communities in response to geochemical perturbations},
author = {Wilpiszeski, Regina L. and Gionfriddo, Caitlin M. and Wymore, Ann M. and Moon, Ji-Won and Lowe, Kenneth A. and Podar, Mircea and Rafie, Sa’ad and Fields, Matthew W. and Hazen, Terry C. and Ge, Xiaoxuan and Poole, Farris and Adams, Michael W. and Chakraborty, Romy and Fan, Yupeng and Van Nostrand, Joy D. and Zhou, Jizhong and Arkin, Adam P. and Elias, Dwayne A.},
abstractNote = {Subsurface microbial communities mediate the transformation and fate of redox sensitive materials including organic matter, metals and radionuclides. Few studies have explored how changing geochemical conditions influence the composition of groundwater microbial communities over time. We temporally monitored alterations in abiotic forces on microbial community structure using 1L in-field bioreactors receiving background and contaminated groundwater at the Oak Ridge Reservation, TN. Planktonic and biofilm microbial communities were initialized with background water for 4 days to establish communities in triplicate control reactors and triplicate test reactors and then fed filtered water for 14 days. On day 18, three reactors were switched to receive filtered groundwater from a contaminated well, enriched in total dissolved solids relative to the background site, particularly chloride, nitrate, uranium, and sulfate. Biological and geochemical data were collected throughout the experiment, including planktonic and biofilm DNA for 16S rRNA amplicon sequencing, cell counts, total protein, anions, cations, trace metals, organic acids, bicarbonate, pH, Eh, DO, and conductivity. We observed significant shifts in both planktonic and biofilm microbial communities receiving contaminated water. This included a loss of rare taxa, especially amongst members of the Bacteroidetes, Acidobacteria, Chloroflexi, and Betaproteobacteria, but enrichment in the Fe- and nitrate- reducing Ferribacterium and parasitic Bdellovibrio. These shifted communities were more similar to the contaminated well community, suggesting that geochemical forces substantially influence microbial community diversity and structure. These influences can only be captured through such comprehensive temporal studies, which also enable more robust and accurate predictive models to be developed.},
doi = {10.1371/journal.pone.0232437},
journal = {PLoS ONE},
number = 9,
volume = 15,
place = {United States},
year = {Mon Sep 28 00:00:00 EDT 2020},
month = {Mon Sep 28 00:00:00 EDT 2020}
}
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Works referenced in this record:
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
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
The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions
journal, September 2004
- O'Day, P. A.; Vlassopoulos, D.; Root, R.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 38
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
The influence of microbial redox cycling on radionuclide mobility in the subsurface at a low-level radioactive waste storage site
journal, September 2007
- Wilkins, M. J.; Livens, F. R.; Vaughan, D. J.
- Geobiology, Vol. 5, Issue 3
Role of metal-reducing bacteria in arsenic release from Bengal delta sediments
journal, July 2004
- Islam, Farhana S.; Gault, Andrew G.; Boothman, Christopher
- Nature, Vol. 430, Issue 6995
The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions
journal, September 2004
- O'Day, P. A.; Vlassopoulos, D.; Root, R.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 38
Sulfate-reducing bacterial community response to carbon source amendments in contaminated aquifer microcosms
journal, October 2002
- Kleikemper, Jutta; Pelz, Oliver; Schroth, Martin H.
- FEMS Microbiology Ecology, Vol. 42, Issue 1
Influence of inorganic and organic nutrients on aerobic biodegradation and on the adaptation response of subsurface microbial communities
journal, January 1988
- Swindoll, C. M.; Aelion, C. M.; Pfaender, F. K.
- Applied and Environmental Microbiology, Vol. 54, Issue 1
Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased
journal, November 2018
- Beattie, Rachelle E.; Henke, Wyatt; Campa, Maria F.
- Soil Biology and Biochemistry, Vol. 126
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
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
Natural Bacterial Communities Serve as Quantitative Geochemical Biosensors
journal, May 2015
- Smith, Mark B.; Rocha, Andrea M.; Smillie, Chris S.
- mBio, Vol. 6, Issue 3
Physicochemical and Mineralogical Characterization of Soil–Saprolite Cores from a Field Research Site, Tennessee
journal, January 2006
- Moon, Ji-Won; Roh, Yul; Phelps, Tommy J.
- Journal of Environment Quality, Vol. 35, Issue 5
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
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
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
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
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
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
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
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
Temporal Dynamics of In-Field Bioreactor Populations Reflect the Groundwater System and Respond Predictably to Perturbation
journal, February 2017
- King, Andrew J.; Preheim, Sarah P.; Bailey, Kathryn L.
- Environmental Science & Technology, Vol. 51, Issue 5
Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site
journal, August 2013
- Chourey, Karuna; Nissen, Silke; Vishnivetskaya, Tatiana
- PROTEOMICS
In Situ Bioreduction of Technetium and Uranium in a Nitrate-Contaminated Aquifer
journal, January 2004
- Istok, J. D.; Senko, J. M.; Krumholz, L. R.
- Environmental Science & Technology, Vol. 38, Issue 2
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
Scalable production of microbially mediated zinc sulfide nanoparticles and application to functional thin films
journal, October 2014
- Moon, Ji-Won; Ivanov, Ilia N.; Joshi, Pooran C.
- Acta Biomaterialia, Vol. 10, Issue 10
PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR
journal, July 1996
- Ahn, S.
- Nucleic Acids Research, Vol. 24, Issue 13
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
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
VSEARCH: a versatile open source tool for metagenomics
journal, January 2016
- Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben
- PeerJ, Vol. 4
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
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
STAMP: statistical analysis of taxonomic and functional profiles
journal, July 2014
- Parks, Donovan H.; Tyson, Gene W.; Hugenholtz, Philip
- Bioinformatics, Vol. 30, Issue 21
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Fate and transport of uranium (VI) in weathered saprolite
journal, January 2015
- Kim, Young-Jin; Brooks, Scott C.; Zhang, Fan
- Journal of Environmental Radioactivity, Vol. 139
Phenylobacterium immobile gen. nov., sp. nov., a Gram-Negative Bacterium That Degrades the Herbicide Chloridazon
journal, January 1985
- Lingens, F.; Blecher, R.; Blecher, H.
- International Journal of Systematic Bacteriology, Vol. 35, Issue 1
Random Forests for Classification in Ecology
journal, November 2007
- Cutler, D. Richard; Edwards, Thomas C.; Beard, Karen H.
- Ecology, Vol. 88, Issue 11
Nitrate-Reducing Bacteria at the Nitrate and Radionuclide Contaminated Oak Ridge Integrated Field Research Challenge Site: A Review
journal, June 2011
- Spain, Anne M.; Krumholz, Lee R.
- Geomicrobiology Journal, Vol. 28, Issue 5-6
Microbial Community and in situ Bioremediation of Groundwater by Nitrate Removal in the Zone of a Radioactive Waste Surface Repository
journal, August 2018
- Safonov, Alexey V.; Babich, Tamara L.; Sokolova, Diyana S.
- Frontiers in Microbiology, Vol. 9
Changes in Microbial Community Composition and Geochemistry during Uranium and Technetium Bioimmobilization
journal, September 2007
- Michalsen, Mandy M.; Peacock, Aaron D.; Spain, Anne M.
- Applied and Environmental Microbiology, Vol. 73, Issue 18
Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing
journal, June 2014
- Leigh, Mary Beth; Wu, Wei-Min; Cardenas, Erick
- Frontiers of Environmental Science & Engineering, Vol. 9, Issue 3
Ferribacterium limneticum , gen. nov., sp. nov., an Fe(III)-reducing microorganism isolated from mining-impacted freshwater lake sediments
journal, February 1999
- Cummings, David E.; Caccavo Jr., Frank; Spring, Stefan
- Archives of Microbiology, Vol. 171, Issue 3
Predatory Lifestyle of Bdellovibrio bacteriovorus
journal, October 2009
- Sockett, Renee Elizabeth
- Annual Review of Microbiology, Vol. 63, Issue 1