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Title: Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols

Abstract

Alcohols are commonly derived from the degradation of organic matter and yet are rarely measured in environmental samples. Wetlands in the Prairie Pothole Region (PPR) support extremely high methane emissions and the highest sulfate reduction rates reported to date, likely contributing to a significant proportion of organic matter mineralization in this system. Here, while ethanol and isopropanol concentrations up to 4 to 5 mM in PPR wetland pore fluids have been implicated in sustaining these high rates of microbial activity, the mechanisms that support alcohol cycling in this ecosystem are poorly understood. We leveraged metagenomic and transcriptomic tools to identify genes, pathways, and microorganisms potentially accounting for alcohol cycling in PPR wetlands. Phylogenetic analyses revealed diverse alcohol dehydrogenases and putative substrates. Alcohol dehydrogenase and aldehyde dehydrogenase genes were included in 62 metagenome-assembled genomes (MAGs) affiliated with 16 phyla.

Authors:
ORCiD logo [1];  [1];  [2];  [2];  [3];  [4]
  1. Radboud Univ. Nijmegen, Nijmegen (The Netherlands)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Colorado State Univ., Fort Collins, CO (United States)
  4. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1567060
Report Number(s):
PNNL-SA-147002
Journal ID: ISSN 0099-2240
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 12; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; wetlands; RNA-Seq; metagenomics; alcohol cycling

Citation Formats

Martins, Paula Dalcin, Frank, Jeroen, Mitchell, Hugh D., Markillie, Lye Meng, Wilkins, Michael J., and Stabb, Eric V. Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols. United States: N. p., 2019. Web. doi:10.1128/AEM.00189-19.
Martins, Paula Dalcin, Frank, Jeroen, Mitchell, Hugh D., Markillie, Lye Meng, Wilkins, Michael J., & Stabb, Eric V. Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols. United States. doi:10.1128/AEM.00189-19.
Martins, Paula Dalcin, Frank, Jeroen, Mitchell, Hugh D., Markillie, Lye Meng, Wilkins, Michael J., and Stabb, Eric V. Thu . "Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols". United States. doi:10.1128/AEM.00189-19. https://www.osti.gov/servlets/purl/1567060.
@article{osti_1567060,
title = {Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols},
author = {Martins, Paula Dalcin and Frank, Jeroen and Mitchell, Hugh D. and Markillie, Lye Meng and Wilkins, Michael J. and Stabb, Eric V.},
abstractNote = {Alcohols are commonly derived from the degradation of organic matter and yet are rarely measured in environmental samples. Wetlands in the Prairie Pothole Region (PPR) support extremely high methane emissions and the highest sulfate reduction rates reported to date, likely contributing to a significant proportion of organic matter mineralization in this system. Here, while ethanol and isopropanol concentrations up to 4 to 5 mM in PPR wetland pore fluids have been implicated in sustaining these high rates of microbial activity, the mechanisms that support alcohol cycling in this ecosystem are poorly understood. We leveraged metagenomic and transcriptomic tools to identify genes, pathways, and microorganisms potentially accounting for alcohol cycling in PPR wetlands. Phylogenetic analyses revealed diverse alcohol dehydrogenases and putative substrates. Alcohol dehydrogenase and aldehyde dehydrogenase genes were included in 62 metagenome-assembled genomes (MAGs) affiliated with 16 phyla.},
doi = {10.1128/AEM.00189-19},
journal = {Applied and Environmental Microbiology},
number = 12,
volume = 85,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 2 works
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Figures / Tables:

FIG 1 FIG 1: Simplified summary of investigated pathways for ethanol and isopropanol production. ATP-generating reactions are indicated by closed circles, and ATP-consuming reactions are indicated by open circles. NAD(P)H-generating reactions are indicated by closed squares. NAD(P)H-consuming reactions are indicated by open squares. Reduced ferredoxin [Fd(red)]-generating reactions are indicated by closed stars.more » Oxidized ferredoxin [Fd(ox)]-generating reactions are indicated by open stars. Solid arrows indicate the written reaction, while dashed arrows indicate a series of reactions not shown. In acetone/isopropanolbutanol- ethanol fermentation, red arrows indicate solventogenic phase reactions, and the green arrow and substrate indicate an additional reaction in the isopropanol-producing variation. In the Pyrococcus furiosus-like fermentation, “R-” indicates the radical in the molecule. Enzymes are numbered as follows: 1, hexokinase; 2, glucose-6-P dehydrogenase; 3, 6-P-gluconate dehydrogenase; 4, ribulose-5-P epimerase; 5, phosphoketolase; 6, glyceraldehyde-3-P dehydrogenase; 7, 3-P-glycerate kinase; 8, 3-P-glycerate mutase; 9, enolase; 10, pyruvate kinase; 11, lactate dehydrogenase; 12, phosphotransacetylase; 13, aldehyde dehydrogenase; 14, alcohol dehydrogenase; 15, phosphoenolpyruvate (PEP) carboxylase; 16, malate dehydrogenase; 17, fumarase; 18, succinate dehydrogenase; 19, pyruvate-formate lyase; 20, formate-hydrogen lyase; 21, acetate kinase; 22, alpha-acetolactate synthase; 23, alpha-acetolactatedecarboxylase; 24, 2,3-butanediol dehydrogenase; 25, PFOR, IFOR, OGFOR, or OIFOR; 26, ferredoxin hydrogenase; 27, acetyl-CoA acetyltransferase; 28, hydroxybutyryl-CoA dehydrogenase; 29, crotonase; 30, butyryl-CoA dehydrogenase; 31, phosphotransbutyrylase; 32, butyrate kinase; 33, butyraldehyde dehydrogenase; 34, butanol dehydrogenase; 35, acetoacetyl-CoA:acetate/butyrate:CoA transferase; 36, acetoacetate decarboxylase; 37, isopropanol dehydrogenase; 38, hydrogen dehydrogenase; 39, aldehyde:ferredoxin oxidoreductase; 40, acetyl-CoA synthetase. Fermentations are not balanced, and reversible reactions are not indicated.« less

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