skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Carbon Amendments Alter Microbial Community Structure and Net Mercury Methylation Potential in Sediments

Journal Article · · Applied and Environmental Microbiology
DOI:https://doi.org/10.1128/AEM.01049-17· OSTI ID:1785153
 [1];  [2];  [3];  [4];  [1];  [5];  [1];  [1];  [1];  [6];  [1];  [7]; ORCiD logo [1];
  1. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  2. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA, Department of Soil and Crop Sciences, Texas A&,M University, Overton, Texas, USA
  3. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA, Department of Chemical and Materials Engineering, University of Idaho, Moscow, Idaho, USA
  4. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA, Department of Biology, Troy University, Troy, Alabama, USA
  5. Smithsonian Environmental Research Center, Edgewater, Maryland, USA
  6. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  7. Department of Biochemistry, University of Missouri, Columbia, Missouri, USA

ABSTRACT Neurotoxic methylmercury (MeHg) is produced by anaerobic Bacteria and Archaea possessing the genes hgcAB , but it is unknown how organic substrate and electron acceptor availability impacts the distribution and abundance of these organisms. We evaluated the impact of organic substrate amendments on mercury (Hg) methylation rates, microbial community structure, and the distribution of hgcAB + microbes with sediments. Sediment slurries were amended with short-chain fatty acids, alcohols, or a polysaccharide. Minimal increases in MeHg were observed following lactate, ethanol, and methanol amendments, while a significant decrease (∼70%) was observed with cellobiose incubations. Postincubation, microbial diversity was assessed via 16S rRNA amplicon sequencing. The presence of hgcAB + organisms was assessed with a broad-range degenerate PCR primer set for both genes, while the presence of microbes in each of the three dominant clades of methylators ( Deltaproteobacteria , Firmicutes , and methanogenic Archaea ) was measured with clade-specific degenerate hgcA quantitative PCR (qPCR) primer sets. The predominant microorganisms in unamended sediments consisted of Proteobacteria , Firmicutes , Bacteroidetes , and Actinobacteria . Clade-specific qPCR identified hgcA + Deltaproteobacteria and Archaea in all sites but failed to detect hgcA + Firmicutes . Cellobiose shifted the communities in all samples to ∼90% non- hgcAB -containing Firmicutes (mainly Bacillus spp. and Clostridium spp.). These results suggest that either expression of hgcAB is downregulated or, more likely given the lack of 16S rRNA gene presence after cellobiose incubation, Hg-methylating organisms are largely outcompeted by cellobiose degraders or degradation products of cellobiose. These results represent a step toward understanding and exploring simple methodologies for controlling MeHg production in the environment. IMPORTANCE Methylmercury (MeHg) is a neurotoxin produced by microorganisms that bioacummulates in the food web and poses a serious health risk to humans. Currently, the impact that organic substrate or electron acceptor availability has on the mercury (Hg)-methylating microorganisms is unclear. To study this, we set up microcosm experiments exposed to different organic substrates and electron acceptors and assayed for Hg methylation rates, for microbial community structure, and for distribution of Hg methylators. The sediment and groundwater was collected from East Fork Poplar Creek in Oak Ridge, TN. Amendment with cellobiose (a lignocellulosic degradation by-product) led to a drastic decrease in the Hg methylation rate compared to that in an unamended control, with an associated shift in the microbial community to mostly nonmethylating Firmicutes . This, along with previous Hg-methylating microorganism identification methods, will be important for identifying strategies to control MeHg production and inform future remediation strategies.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1785153
Alternate ID(s):
OSTI ID: 1423062
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Vol. 84 Journal Issue: 3; ISSN 0099-2240
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 31 works
Citation information provided by
Web of Science

References (52)

Methanogens: Principal Methylators of Mercury in Lake Periphyton journal September 2011
Assessing sulfate and carbon controls on net methylmercury production in peatlands: An in situ mesocosm approach journal March 2008
Development and Validation of Broad-Range Qualitative and Clade-Specific Quantitative Molecular Probes for Assessing Mercury Methylation in the Environment journal July 2016
Microbial Mercury Transformation in Anoxic Freshwater Sediments under Iron-Reducing and Other Electron-Accepting Conditions journal May 2003
Methylation and demethylation of mercury under controlled redox, pH and salinity conditions. journal January 1984
Long-term increased bioaccumulation of mercury in largemouth bass follows reduction of waterborne selenium journal October 2000
Sequencing Intractable DNA to Close Microbial Genomes journal July 2012
Sulfide Controls on Mercury Speciation and Bioavailability to Methylating Bacteria in Sediment Pore Waters journal March 1999
Third Generation Biofuels via Direct Cellulose Fermentation journal July 2008
Mercury Methylation by Novel Microorganisms from New Environments journal September 2013
Effect of point source removal on mercury bioaccumulation in an industrial pond journal November 2002
Genome of Geobacter sulfurreducens: Metal Reduction in Subsurface Environments journal December 2003
Mercury Methylation by Interspecies Hydrogen and Acetate Transfer between Sulfidogens and Methanogens journal June 1998
Decrease in Net Mercury Methylation Rates Following Iron Amendment to Anoxic Wetland Sediment Slurries journal April 2005
Mercury and Other Heavy Metals Influence Bacterial Community Structure in Contaminated Tennessee Streams journal November 2010
Hydrologic indicators of hot spots and hot moments of mercury methylation potential along river corridors journal October 2016
Contribution of Coexisting Sulfate and Iron Reducing Bacteria to Methylmercury Production in Freshwater River Sediments journal February 2012
Ribosomal Database Project: data and tools for high throughput rRNA analysis journal November 2013
Relationships between bacterial energetic metabolism, mercury methylation potential, and hgcA/hgcB gene expression in Desulfovibrio dechloroacetivorans BerOc1 journal March 2015
Characterization of Archaeal Community in Contaminated and Uncontaminated Surface Stream Sediments journal August 2010
The Genetic Basis for Bacterial Mercury Methylation journal February 2013
Role of Morphological Growth State and Gene Expression in Desulfovibrio africanus Strain Walvis Bay Mercury Methylation journal April 2012
Global prevalence and distribution of genes and microorganisms involved in mercury methylation journal October 2015
Accumulation of total mercury and methylmercury in rice plants collected from different mining areas in China journal January 2014
Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities: Metagenomic and rRNA diversity characterization journal February 2013
A new mathematical model for relative quantification in real-time RT-PCR journal May 2001
History of mercury use and environmental contamination at the Oak Ridge Y-12 Plant journal January 2011
Improved Yield of High Molecular Weight DNA Coincides with Increased Microbial Diversity Access from Iron Oxide Cemented Sub-Surface Clay Environments journal July 2014
Removing Noise From Pyrosequenced Amplicons journal January 2011
Genome Sequence of the Mercury-Methylating Strain Desulfovibrio desulfuricans ND132 journal February 2011
Characterization of the Deltaproteobacteria in contaminated and uncontaminated stream sediments and identification of potential mercury methylators journal July 2012
Characterization of Microbial Activities and U Reduction in a Shallow Aquifer Contaminated by Uranium Mill Tailings journal July 2003
Artifact formation of methyl mercury during aqueous distillation and alternative techniques for the extraction of methyl mercury from environmental samples journal June 1997
Measurement of Complexation of Methylmercury(II) Compounds by Freshwater Humic Substances Using Equilibrium Dialysis journal February 1997
Mercury Methylation from Unexpected Sources: Molybdate-Inhibited Freshwater Sediments and an Iron-Reducing Bacterium journal January 2006
Microbial Cellulose Utilization: Fundamentals and Biotechnology journal September 2002
Sulfate Addition Increases Methylmercury Production in an Experimental Wetland journal June 2006
Mercury Methylation by the Methanogen Methanospirillum hungatei journal August 2013
Methylmercury production in sediment from agricultural and non-agricultural wetlands in the Yolo Bypass, California, USA journal June 2014
The effects of a stannous chloride-based water treatment system in a mercury contaminated stream journal November 2015
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities journal October 2009
Basic local alignment search tool journal October 1990
QIIME allows analysis of high-throughput community sequencing data journal April 2010
Geochemical Controls on the Production and Distribution of Methylmercury in Near-Shore Marine Sediments journal March 2004
Methanogens: a surprising microbial group journal January 1979
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix journal April 2009
Bioaccumulation of mercury and methylmercury journal February 1995
Mechanisms Regulating Mercury Bioavailability for Methylating Microorganisms in the Aquatic Environment: A Critical Review journal February 2013
Mercury methylation in aquatic systems affected by acid deposition journal January 1991
Estimation of mercury-sulfide speciation in sediment pore waters using octanol-water partitioning and implications for availability to methylating bacteria: Mercury-sulfide speciation journal October 1999
Bioaccumulation Factors for Mercury in Stream Fish journal June 2004