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

Title: The selective pressures on the microbial community in a metal-contaminated aquifer

Journal Article · · The ISME Journal

Abstract In many environments, toxic compounds restrict which microorganisms persist. However, in complex mixtures of inhibitory compounds, it is challenging to determine which specific compounds cause changes in abundance and prevent some microorganisms from growing. We focused on a contaminated aquifer in Oak Ridge, Tennessee, USA that has large gradients of pH and widely varying concentrations of uranium, nitrate, and many other inorganic ions. In the most contaminated wells, the microbial community is enriched in the Rhodanobacter genus. Rhodanobacter abundance is positively correlated with low pH and high concentrations of uranium and 13 other ions and we sought to determine which of these ions are selective pressures that favor the growth of Rhodanobacter over other taxa. Of these ions, low pH and high UO22+, Mn2+, Al3+, Cd2+, Zn2+, Co2+, and Ni2+ are both (a) selectively inhibitory of a Pseudomonas isolate from an uncontaminated well vs. a Rhodanobacter isolate from a contaminated well, and (b) reach toxic concentrations (for the Pseudomonas isolate) in the Rhodanobacter-dominated wells. We used mixtures of ions to simulate the groundwater conditions in the most contaminated wells and verified that few isolates aside from Rhodanobacter can tolerate these eight ions. These results clarify which ions are likely causal factors that impact the microbial community at this field site and are not merely correlated with taxonomic shifts. Furthermore, our general high-throughput approach can be applied to other environments, isolates, and conditions to systematically help identify selective pressures on microbial communities.

Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231; AC02-05CH11231
OSTI ID:
1619784
Journal Information:
The ISME Journal, Journal Name: The ISME Journal Journal Issue: 4 Vol. 13; ISSN 1751-7362
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (48)

UO 2 2+ speciation determines uranium toxicity and bioaccumulation in an environmental Pseudomonas sp. isolate journal April 2010
Ecological Aspects of Heavy Metal Responses in Microorganisms book January 1985
Complexation of trace metals by adsorbed natural organic matter journal April 1984
The “North American shale composite”: Its compilation, major and trace element characteristics journal December 1984
pH-Dependent uranium toxicity to freshwater hydra journal September 1992
Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review journal September 1998
Microbial communities in acid mine drainage journal May 2003
Historical trends of metals in the sediments of San Francisco Bay, California journal February 1999
The microbiology of acidic mine waters journal September 2003
Toxicity of uranium and copper individually, and in combination, to a tropical freshwater macrophyte (Lemna aequinoctialis) journal March 2006
Bioremediation of uranium-contaminated groundwater: a systems approach to subsurface biogeochemistry journal June 2013
The use of chelating agents in the remediation of metal-contaminated soils: A review journal May 2008
Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid–uranium waste journal August 2005
Determination of metals and metalloids in light and heavy crude oil by ICP-MS after digestion by microwave-induced combustion journal September 2010
High-Throughput Screening To Identify Potent and Specific Inhibitors of Microbial Sulfate Reduction journal May 2017
Mobility of natural organic matter in a study aquifer journal April 1993
Elevated Microbial Tolerance to Metals and Antibiotics in Metal-Contaminated Industrial Environments journal May 2005
In Situ Bioremediation of Uranium with Emulsified Vegetable Oil as the Electron Donor journal May 2013
Monofluorophosphate Is a Selective Inhibitor of Respiratory Sulfate-Reducing Microorganisms journal February 2015
Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review journal January 2003
Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community journal February 2010
Spatial and temporal dynamics of the microbial community in the Hanford unconfined aquifer journal March 2012
Aquifer environment selects for microbial species cohorts in sediment and groundwater journal February 2015
Embracing the unknown: disentangling the complexities of the soil microbiome journal August 2017
Antimicrobial activity of metals: mechanisms, molecular targets and applications journal May 2013
Mutant phenotypes for thousands of bacterial genes of unknown function journal May 2018
Proterozoic ocean redox and biogeochemical stasis journal March 2013
Conceptual Synthesis in Community Ecology journal June 2010
Metal speciation and microbial growth--the hard (and soft) facts journal April 1991
Metals, minerals and microbes: geomicrobiology and bioremediation journal December 2009
Niche dimensionality links biodiversity and invasibility of microbial communities journal October 2012
Pseudomonas fluorescens' view of the periodic table journal September 2007
Denitrification at pH 4 by a soil-derived Rhodanobacter-dominated community: Denitrification at pH 4 journal December 2010
Minerals in soil select distinct bacterial communities in their microhabitats: Interactions between minerals and bacteria in soil journal March 2009
Prospects for harnessing biocide resistance for bioremediation and detoxification journal May 2018
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal June 2007
Molybdenum Availability Is Key to Nitrate Removal in Contaminated Groundwater Environments journal May 2015
Bacterial Community Shift and Coexisting/Coexcluding Patterns Revealed by Network Analysis in a Uranium-Contaminated Site after Bioreduction Followed by Reoxidation journal February 2018
Denitrifying Bacteria from the Genus Rhodanobacter Dominate Bacterial Communities in the Highly Contaminated Subsurface of a Nuclear Legacy Waste Site journal December 2011
Natural Bacterial Communities Serve as Quantitative Geochemical Biosensors journal May 2015
Lateral Gene Transfer in a Heavy Metal-Contaminated-Groundwater Microbial Community journal April 2016
Microbial metal resistance and metabolism across dynamic landscapes: high-throughput environmental microbiology journal January 2017
Dose-Response Analysis Using R journal December 2015
Bioassay Analysis using R journal January 2005
Fate of Natural Organic Matter (NOM) during Groundwater Recharge using Reclaimed Water journal November 1999
Comparative metagenomics reveals impact of contaminants on groundwater microbiomes journal October 2015
Mechanisms of Chromium and Uranium Toxicity in Pseudomonas stutzeri RCH2 Grown under Anaerobic Nitrate-Reducing Conditions journal August 2017
Microbial Interactions With Dissolved Organic Matter Drive Carbon Dynamics and Community Succession journal June 2018