Incorporating concentration-dependent sediment microbial activity into methylmercury production kinetics modeling

Schwartz, Grace E.; Muller, Katherine A.; Rathore, Saubhagya S.; Wilpiszeski, Regina L.; Carrell, Alyssa A.; Cregger, Melissa A.; Elias, Dwayne A.; Podar, Mircea; Painter, Scott L.; Brooks, Scott C.

doi:10.1039/d1em00287b

Title: Incorporating concentration-dependent sediment microbial activity into methylmercury production kinetics modeling

Journal Article · Fri Oct 29 00:00:00 UTC 2021 · Environmental Science: Processes & Impacts

DOI: https://doi.org/10.1039/d1em00287b · OSTI ID:1873838

^[1]; Muller, Katherine A. ^[2];

^[1]; Wilpiszeski, Regina L. ^[1]; Carrell, Alyssa A. ^[1];

^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

We report in anoxic environments, anaerobic microorganisms carrying the hgcAB gene cluster can mediate the transformation of inorganic mercury (Hg(II)) to monomethylmercury (MMHg). The kinetics of Hg(II) transformation to MMHg in periphyton from East Fork Poplar Creek (EFPC) in Oak Ridge, TN have previously been modeled using a transient availability model (TAM). The TAM for Hg(II) methylation combines methylation/demethylation kinetics with kinetic expressions for processes that decrease Hg(II) and MMHg availability for methylation and demethylation (multisite sorption of Hg(II) and MMHg, Hg(II) reduction/Hg(0) oxidation). In this study, the TAM is used for the first time to describe MMHg production in sediment. We assessed MMHg production in sediment microcosms using two different sediment types from EFPC: a relatively anoxic, carbon-rich sediment with higher microbial activity (higher CO₂ production from sediment) and a relatively oxic, sandy, carbon-poor sediment with lower microbial activity (lower CO₂ production from sediment). Based on 16s rRNA sequencing, the overall microbial community structure in the two sediments was retained during the incubations. However, the hgcA containing methanogenic Euryarchaeota communities differed between sediment types and their growth followed different trajectories over the course of incubations, potentially contributing to the distinct patterns of MMHg production observed. The general TAM paradigm performed well in describing MMHg production in the sediments. However, the MMHg production and ancillary data suggested the need to revise the model structure to incorporate terms for concentration-dependent microbial activity over the course of the incubations. We modified the TAM to include Monod-type kinetics for methylation and demethylation and observed an improved fit for the carbon-rich, microbially active sediment. Overall our work shows that the TAM can be applied to describe Hg(II) methylation in sediments and that including expressions accounting for concentration-dependent microbial activity can improve the accuracy of the model description of the data in some cases.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; AC05-76RL01830

OSTI ID:: 1873838

Report Number(s):: PNNL-SA-164700

Journal Information:: Environmental Science: Processes & Impacts, Journal Name: Environmental Science: Processes & Impacts Vol. 24; ISSN 2050-7887

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

High-yield synthesis of milligram amounts of isotopically enriched methylmercury(CH3198HgCl) Bancon-Montigny, Chrystelle; Yang, Lu; Sturgeon, Ralph E. Applied Organometallic Chemistry, Vol. 18, Issue 2 https://doi.org/10.1002/aoc.572	journal	January 2004
Seasonal and flow-driven dynamics of particulate and dissolved mercury and methylmercury in a stream impacted by an industrial mercury source: Hg and MeHg dynamics in an industrially contaminated stream Riscassi, Ami; Miller, Carrie; Brooks, Scott Environmental Toxicology and Chemistry, Vol. 35, Issue 6 https://doi.org/10.1002/etc.3310	journal	March 2016
Ecosystem Controls on Methylmercury Production by Periphyton Biofilms in a Contaminated Stream: Implications for Predictive Modeling Schwartz, Grace E.; Olsen, Todd A.; Muller, Katherine A. Environmental Toxicology and Chemistry, Vol. 38, Issue 11 https://doi.org/10.1002/etc.4551	journal	September 2019
Constants of mercury methylation and demethylation rates in sediments and comparison of tracer and ambient mercury availability Hintelmann, Holger; Keppel-Jones, Katherine; Evans, R. Douglas Environmental Toxicology and Chemistry, Vol. 19, Issue 9 https://doi.org/10.1002/etc.5620190909	journal	September 2000
ggplot2: ggplot2 Wickham, Hadley Wiley Interdisciplinary Reviews: Computational Statistics, Vol. 3, Issue 2 https://doi.org/10.1002/wics.147	journal	February 2011
Artifact formation of methyl mercury during aqueous distillation and alternative techniques for the extraction of methyl mercury from environmental samples Bloom, N. S.; Colman, John A.; Barber, Lee Fresenius' Journal of Analytical Chemistry, Vol. 358, Issue 3 https://doi.org/10.1007/s002160050432	journal	June 1997
Relationships between bacterial energetic metabolism, mercury methylation potential, and hgcA/hgcB gene expression in Desulfovibrio dechloroacetivorans BerOc1 Goñi-Urriza, Marisol; Corsellis, Yannick; Lanceleur, Laurent Environmental Science and Pollution Research, Vol. 22, Issue 18 https://doi.org/10.1007/s11356-015-4273-5	journal	March 2015
Persistent Hg contamination and occurrence of Hg-methylating transcript (hgcA) downstream of a chlor-alkali plant in the Olt River (Romania) Bravo, Andrea G.; Loizeau, Jean-Luc; Dranguet, Perrine Environmental Science and Pollution Research, Vol. 23, Issue 11 https://doi.org/10.1007/s11356-015-5906-4	journal	December 2015
History of mercury use and environmental contamination at the Oak Ridge Y-12 Plant Brooks, Scott C.; Southworth, George R. Environmental Pollution, Vol. 159, Issue 1 https://doi.org/10.1016/j.envpol.2010.09.009	journal	January 2011
Formation and mobilization of methylmercury across natural and experimental sulfur deposition gradients Åkerblom, Staffan; Nilsson, Mats B.; Skyllberg, Ulf Environmental Pollution, Vol. 263 https://doi.org/10.1016/j.envpol.2020.114398	journal	August 2020
Dissolution of cinnabar (HgS) in the presence of natural organic matter Waples, Jacob S.; Nagy, Kathryn L.; Aiken, George R. Geochimica et Cosmochimica Acta, Vol. 69, Issue 6 https://doi.org/10.1016/j.gca.2004.09.029	journal	March 2005
Enhanced availability of mercury bound to dissolved organic matter for methylation in marine sediments Mazrui, Nashaat M.; Jonsson, Sofi; Thota, Sravan Geochimica et Cosmochimica Acta, Vol. 194 https://doi.org/10.1016/j.gca.2016.08.019	journal	December 2016
Fate and transport of uranium (VI) in weathered saprolite Kim, Young-Jin; Brooks, Scott C.; Zhang, Fan Journal of Environmental Radioactivity, Vol. 139 https://doi.org/10.1016/j.jenvrad.2014.10.008	journal	January 2015
Mercury methylation/demethylation and volatilization pathways in estuarine sediment slurries using species-specific enriched stable isotopes Rodrı́guez Martı́n-Doimeadios, R. C.; Tessier, E.; Amouroux, D. Marine Chemistry, Vol. 90, Issue 1-4 https://doi.org/10.1016/j.marchem.2004.02.022	journal	November 2004
Organic matter and sulfide inhibit methylmercury production in sediments of New York/New Jersey Harbor Hammerschmidt, Chad R.; Fitzgerald, William F.; Balcom, Prentiss H. Marine Chemistry, Vol. 109, Issue 1-2 https://doi.org/10.1016/j.marchem.2008.01.007	journal	February 2008
Importance of organic matter lability for monomethylmercury production in sulfate-rich marine sediments Kim, Miji; Han, Seunghee; Gieskes, Joris Science of The Total Environment, Vol. 409, Issue 4 https://doi.org/10.1016/j.scitotenv.2010.10.050	journal	January 2011
Biogeochemical factors influencing net mercury methylation in contaminated freshwater sediments from the St. Lawrence River in Cornwall, Ontario, Canada Avramescu, Mary-Luyza; Yumvihoze, Emmanuel; Hintelmann, Holger Science of The Total Environment, Vol. 409, Issue 5 https://doi.org/10.1016/j.scitotenv.2010.11.016	journal	February 2011
Distribution and biogeochemical controls on net methylmercury production in Penobscot River marshes and sediment Gilmour, Cynthia; Bell, James Tyler; Soren, Ally Bullock Science of The Total Environment, Vol. 640-641 https://doi.org/10.1016/j.scitotenv.2018.05.276	journal	November 2018
The assessment and remediation of mercury contaminated sites: A review of current approaches Eckley, Chris S.; Gilmour, Cynthia C.; Janssen, Sarah Science of The Total Environment, Vol. 707 https://doi.org/10.1016/j.scitotenv.2019.136031	journal	March 2020
Mercury cycling in freshwater systems - An updated conceptual model Branfireun, Brian A.; Cosio, Claudia; Poulain, Alexandre J. Science of The Total Environment, Vol. 745 https://doi.org/10.1016/j.scitotenv.2020.140906	journal	November 2020
Ferrozine---a new spectrophotometric reagent for iron Stookey, Lawrence L. Analytical Chemistry, Vol. 42, Issue 7, p. 779-781 https://doi.org/10.1021/ac60289a016	journal	June 1970
Dimethylmercury Degradation by Dissolved Sulfide and Mackinawite West, Johannes; Graham, Andrew M.; Liem-Nguyen, Van Environmental Science & Technology, Vol. 54, Issue 21 https://doi.org/10.1021/acs.est.0c04134	journal	October 2020
Effects of Nutrient Loading and Mercury Chemical Speciation on the Formation and Degradation of Methylmercury in Estuarine Sediment Liem-Nguyen, Van; Jonsson, Sofi; Skyllberg, Ulf Environmental Science & Technology, Vol. 50, Issue 13 https://doi.org/10.1021/acs.est.6b01567	journal	June 2016
Sulfurization of Dissolved Organic Matter Increases Hg–Sulfide–Dissolved Organic Matter Bioavailability to a Hg-Methylating Bacterium Graham, Andrew M.; Cameron-Burr, Keaton T.; Hajic, Hayley A. Environmental Science & Technology, Vol. 51, Issue 16 https://doi.org/10.1021/acs.est.7b02781	journal	July 2017
Kinetics of Methylmercury Production Revisited Olsen, Todd A.; Muller, Katherine A.; Painter, Scott L. Environmental Science & Technology, Vol. 52, Issue 4 https://doi.org/10.1021/acs.est.7b05152	journal	January 2018
Mercury Sorption and Desorption on Organo-Mineral Particulates as a Source for Microbial Methylation Zhang, Lijie; Wu, Shan; Zhao, Linduo Environmental Science & Technology, Vol. 53, Issue 5 https://doi.org/10.1021/acs.est.8b06020	journal	January 2019
Determining the Reliability of Measuring Mercury Cycling Gene Abundance with Correlations with Mercury and Methylmercury Concentrations Christensen, Geoff A.; Gionfriddo, Caitlin M.; King, Andrew J. Environmental Science & Technology, Vol. 53, Issue 15 https://doi.org/10.1021/acs.est.8b06389	journal	July 2019
Mercury Adsorption on Minerals and Its Effect on Microbial Methylation Zhao, Linduo; Li, Yunzi; Zhang, Lijie ACS Earth and Space Chemistry, Vol. 3, Issue 7 https://doi.org/10.1021/acsearthspacechem.9b00039	journal	May 2019
Significance of Kinetics for Sorption on Inorganic Colloids: Modeling and Experiment Interpretation Issues Painter, S.; Cvetkovic, V.; Pickett, D. Environmental Science & Technology, Vol. 36, Issue 24 https://doi.org/10.1021/es025718o	journal	November 2002
Influence of Dissolved Organic Matter on the Environmental Fate of Metals, Nanoparticles, and Colloids Aiken, George R.; Hsu-Kim, Heileen; Ryan, Joseph N. Environmental Science & Technology, Vol. 45, Issue 8 https://doi.org/10.1021/es103992s	journal	April 2011
Dissolved Organic Matter Enhances Microbial Mercury Methylation Under Sulfidic Conditions Graham, Andrew M.; Aiken, George R.; Gilmour, Cynthia C. Environmental Science & Technology, Vol. 46, Issue 5 https://doi.org/10.1021/es203658f	journal	February 2012
Mercury Methylation Rates for Geochemically Relevant Hg ^II Species in Sediments Jonsson, Sofi; Skyllberg, Ulf; Nilsson, Mats B. Environmental Science & Technology, Vol. 46, Issue 21 https://doi.org/10.1021/es3015327	journal	October 2012
Methylmercury Production in Estuarine Sediments: Role of Organic Matter Schartup, Amina T.; Mason, Robert P.; Balcom, Prentiss H. Environmental Science & Technology, Vol. 47, Issue 2 https://doi.org/10.1021/es302566w	journal	December 2012
Mechanisms Regulating Mercury Bioavailability for Methylating Microorganisms in the Aquatic Environment: A Critical Review Hsu-Kim, Heileen; Kucharzyk, Katarzyna H.; Zhang, Tong Environmental Science & Technology, Vol. 47, Issue 6 https://doi.org/10.1021/es304370g	journal	February 2013
Effect of Dissolved Organic Matter Source and Character on Microbial Hg Methylation in Hg–S–DOM Solutions Graham, Andrew M.; Aiken, George R.; Gilmour, Cynthia C. Environmental Science & Technology, Vol. 47, Issue 11 https://doi.org/10.1021/es400414a	journal	May 2013
Mercury Methylation by Novel Microorganisms from New Environments Gilmour, Cynthia C.; Podar, Mircea; Bullock, Allyson L. Environmental Science & Technology, Vol. 47, Issue 20 https://doi.org/10.1021/es403075t	journal	September 2013
Bioavailability of Sediment-Bound Methyl and Inorganic Mercury to a Marine Bivalve Gagnon, Christian; Fisher, Nicholas S. Environmental Science & Technology, Vol. 31, Issue 4 https://doi.org/10.1021/es960364k	journal	April 1997
Inhibition of Precipitation and Aggregation of Metacinnabar (Mercuric Sulfide) by Dissolved Organic Matter Isolated from the Florida Everglades Ravichandran, Mahalingam; Aiken, George R.; Ryan, Joseph N. Environmental Science & Technology, Vol. 33, Issue 9 https://doi.org/10.1021/es9811187	journal	May 1999
Differentiated availability of geochemical mercury pools controls methylmercury levels in estuarine sediment and biota Jonsson, Sofi; Skyllberg, Ulf; Nilsson, Mats B. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5624	journal	August 2014
Practical innovations for high-throughput amplicon sequencing Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2634	journal	September 2013
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Dimethylmercury Formation Mediated by Inorganic and Organic Reduced Sulfur Surfaces Jonsson, Sofi; Mazrui, Nashaat M.; Mason, Robert P. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27958	journal	June 2016
The Toxicology of Mercury — Current Exposures and Clinical Manifestations Clarkson, Thomas W.; Magos, Laszlo; Myers, Gary J. New England Journal of Medicine, Vol. 349, Issue 18 https://doi.org/10.1056/NEJMra022471	journal	October 2003
Effectiveness of Sorbents to Reduce Mercury Methylation Muller, Katherine A.; Brooks, Scott C. Environmental Engineering Science, Vol. 36, Issue 3 https://doi.org/10.1089/ees.2018.0375	journal	March 2019
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Global prevalence and distribution of genes and microorganisms involved in mercury methylation Podar, Mircea; Gilmour, Cynthia C.; Brandt, Craig C. Science Advances, Vol. 1, Issue 9 https://doi.org/10.1126/sciadv.1500675	journal	October 2015
The Genetic Basis for Bacterial Mercury Methylation Parks, J. M.; Johs, A.; Podar, M. Science, Vol. 339, Issue 6125, p. 1332-1335 https://doi.org/10.1126/science.1230667	journal	February 2013
Carbon Amendments Alter Microbial Community Structure and Net Mercury Methylation Potential in Sediments Christensen, Geoff A.; Somenahally, Anil C.; Moberly, James G. Applied and Environmental Microbiology, Vol. 84, Issue 3 https://doi.org/10.1128/AEM.01049-17	journal	November 2017
Mercury and Other Heavy Metals Influence Bacterial Community Structure in Contaminated Tennessee Streams Vishnivetskaya, Tatiana A.; Mosher, Jennifer J.; Palumbo, Anthony V. Applied and Environmental Microbiology, Vol. 77, Issue 1 https://doi.org/10.1128/AEM.01715-10	journal	November 2010
Sulfate-Reducing Bacterium Desulfovibrio desulfuricans ND132 as a Model for Understanding Bacterial Mercury Methylation Gilmour, Cynthia C.; Elias, Dwayne A.; Kucken, Amy M. Applied and Environmental Microbiology, Vol. 77, Issue 12, p. 3938-3951 https://doi.org/10.1128/AEM.02993-10	journal	April 2011
Robust Mercury Methylation across Diverse Methanogenic Archaea Gilmour, Cynthia C.; Bullock, Allyson L.; McBurney, Alyssa mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mBio.02403-17	journal	April 2018
Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times Liang, Xiaoyu; Whitham, Jason M.; Holwerda, Evert K. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1238-1	journal	September 2018
Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin Bokulich, Nicholas A.; Kaehler, Benjamin D.; Rideout, Jai Ram Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0470-z	journal	May 2018
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Methylmercury Exposure and Health Effects in Humans: A Worldwide Concern Mergler, Donna; Anderson, Henry A.; Chan, Laurie Hing Man AMBIO: A Journal of the Human Environment, Vol. 36, Issue 1 https://doi.org/10.1579/0044-7447(2007)36[3:MEAHEI]2.0.CO;2	journal	February 2007
Characterization of the Deltaproteobacteria in contaminated and uncontaminated stream sediments and identification of potential mercury methylators Mosher, Jj; Vishnivetskaya, Ta; Elias, Da Aquatic Microbial Ecology, Vol. 66, Issue 3 https://doi.org/10.3354/ame01563	journal	July 2012
An Improved hgcAB Primer Set and Direct High-Throughput Sequencing Expand Hg-Methylator Diversity in Nature Gionfriddo, Caitlin M.; Wymore, Ann M.; Jones, Daniel S. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.541554	journal	October 2020

Similar Records

Periphyton biofilms influence net methylmercury production in an industrially contaminated system

Journal Article · Mon Sep 12 00:00:00 UTC 2016 · Environmental Science and Technology · OSTI ID:1326487

Olsen, Todd Andrew; Brandt, Craig C.; Brooks, Scott C.

Biotic and abiotic mercury methylation and demethylation in sediments

Journal Article · Sun May 01 04:00:00 UTC 1994 · Bulletin of Environmental Contamination and Toxicology; (United States) · OSTI ID:6759671

Zhang, L; Planas, D

Kinetics of Methylmercury Production Revisited

Journal Article · Sat Jan 27 00:00:00 UTC 2018 · Environmental Science and Technology · OSTI ID:1423042

Olsen, Todd A.; Muller, Katherine A.; Painter, Scott L.; +1 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Monod
kinetics
methylmercury
sediment
transient availability

Title: Incorporating concentration-dependent sediment microbial activity into methylmercury production kinetics modeling

Citation Formats

References (60)

Similar Records

Related Subjects