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

Abstract

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 tomore » ∼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.« less

Authors:

Christensen, Geoff A. ^[1]; Somenahally, Anil C. ^[2]; Moberly, James G. ^[3]; Miller, Carrie M. ^[4]; King, Andrew J. ^[1]; Gilmour, Cynthia C. ^[5]; Brown, Steven D. ^[1]; Podar, Mircea ^[1]; Brandt, Craig C. ^[1]; Brooks, Scott C. ^[6]; Palumbo, Anthony V. ^[1]; Wall, Judy D. ^[7]; Elias, Dwayne A.  ^[1];

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Liu, ed., Shuang-Jiang

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+ Show Author Affiliations

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

Publication Date:

Thu Feb 01 00:00:00 EST 2018

Research Org.:

Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1785153

Alternate Identifier(s):

OSTI ID: 1423062

Grant/Contract Number:  

AC05-00OR22725

Resource Type:

Published Article

Journal Name:

Applied and Environmental Microbiology

Additional Journal Information:

Journal Name: Applied and Environmental Microbiology Journal Volume: 84 Journal Issue: 3; Journal ID: ISSN 0099-2240

Publisher:

American Society for Microbiology

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; methylmercury; 16S; qPCR; hgcA; hgcAB; mercury