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Title: Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Abstract

Wetland soils are one of the largest natural contributors to the emission of methane, a potent greenhouse gas. Currently, microbial contributions to methane emissions from these systems emphasize the roles of acetoclastic and hydrogenotrophic methanogens, while less frequently considering methyl-group substrates (e.g., methanol and methylamines). Here, we integrated laboratory and field experiments to explore the potential for methylotrophic methanogenesis in Old Woman Creek (OWC), a temperate freshwater wetland located in Ohio, USA. We first demonstrated the capacity for methylotrophic methanogenesis in these soils using laboratory soil microcosms amended with trimethylamine. However, subsequent field porewater nuclear magnetic resonance (NMR) analyses to identify methanogenic substrates failed to detect evidence for methylamine compounds in soil porewaters, instead noting the presence of the methylotrophic substrate methanol. Accordingly, our wetland soil-derived metatranscriptomic data indicated that methanol utilization by theMethanomassiliicoccaceaewas the likely source of methylotrophic methanogenesis.Methanomassiliicoccaceaerelative contributions tomcrAtranscripts nearly doubled with depth, accounting for up to 8% of themcrAtranscripts in 25-cm-deep soils. Longitudinal 16S rRNA amplicon andmcrAgene surveys demonstrated thatMethanomassiliicoccaceaewere stably present over 2 years across lateral and depth gradients in this wetland. Meta-analysis of 16S rRNA sequences similar (>99%) to OWCMethanomassiliicoccaceaein public databases revealed a global distribution, with a high representation in terrestrial soils andmore » sediments. Together, our results demonstrate that methylotrophic methanogenesis likely contributes to methane flux from climatically relevant wetland soils. IMPORTANCEUnderstanding the sources and controls on microbial methane production from wetland soils is critical to global methane emission predictions, particularly in light of changing climatic conditions. Current biogeochemical models of methanogenesis consider only acetoclastic and hydrogenotrophic sources and exclude methylotrophic methanogenesis, potentially underestimating microbial contributions to methane flux. Our multi-omic results demonstrated that methylotrophic methanogens of the familyMethanomassiliicoccaceaewere present and active in a freshwater wetland, with metatranscripts indicating that methanol, not methylamines, was the likely substrate under the conditions measured here. However, laboratory experiments indicated the potential for other methanogens to become enriched in response to trimethylamine, revealing the reservoir of methylotrophic methanogenesis potential residing in these soils. Collectively, our approach used coupled field and laboratory investigations to illuminate metabolisms influencing the terrestrial microbial methane cycle, thereby offering direction for increased realism in predictive process-oriented models of methane flux in wetland soils.« less

Authors:
ORCiD logo [1];  [1];  [2]; ORCiD logo [3];  [1];  [3];  [2];  [2];  [3];  [3];  [4]; ORCiD logo [5];  [6];  [7]
  1. Colorado State Univ., Fort Collins, CO (United States). Dept. of Soil and Crop Sciences
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. The Ohio State Univ., Columbus, OH (United States), Dept. of Microbiology
  4. The Ohio State Univ., Columbus, OH (United States), Dept. of Civil, Environmental & Geodetic Engineering
  5. Univ. of Colorado Denver, Colorado (United States), Dept. of Integrative Biology
  6. Colorado State Univ., Fort Collins, CO (United States), Dept. of Soil and Crop Sciences
  7. Woods Hole Oceanographic Institution
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Battelle Memorial Institute, Columbus, OH (United States); The Ohio State Univ., Columbus, OH (United States); Colorado State Univ., Fort Collins, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
EMSL, JGI
OSTI Identifier:
1626180
Alternate Identifier(s):
OSTI ID: 1658627
Grant/Contract Number:  
AC02-05CH11231; AC05-76RL01830; SC0018022; SC0019746
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
Microbiology; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Narrowe, Adrienne B., Borton, Mikayla A., Hoyt, David W., Smith, Garrett J., Daly, Rebecca A., Angle, Jordan C., Eder, Elizabeth K., Wong, Allison R., Wolfe, Richard A., Pappas, Alexandra, Bohrer, Gil, Miller, Christopher S., Wrighton, Kelly C., and Orsi, William. Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils. United States: N. p., 2019. Web. https://doi.org/10.1128/msystems.00320-19.
Narrowe, Adrienne B., Borton, Mikayla A., Hoyt, David W., Smith, Garrett J., Daly, Rebecca A., Angle, Jordan C., Eder, Elizabeth K., Wong, Allison R., Wolfe, Richard A., Pappas, Alexandra, Bohrer, Gil, Miller, Christopher S., Wrighton, Kelly C., & Orsi, William. Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils. United States. https://doi.org/10.1128/msystems.00320-19
Narrowe, Adrienne B., Borton, Mikayla A., Hoyt, David W., Smith, Garrett J., Daly, Rebecca A., Angle, Jordan C., Eder, Elizabeth K., Wong, Allison R., Wolfe, Richard A., Pappas, Alexandra, Bohrer, Gil, Miller, Christopher S., Wrighton, Kelly C., and Orsi, William. Tue . "Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils". United States. https://doi.org/10.1128/msystems.00320-19. https://www.osti.gov/servlets/purl/1626180.
@article{osti_1626180,
title = {Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils},
author = {Narrowe, Adrienne B. and Borton, Mikayla A. and Hoyt, David W. and Smith, Garrett J. and Daly, Rebecca A. and Angle, Jordan C. and Eder, Elizabeth K. and Wong, Allison R. and Wolfe, Richard A. and Pappas, Alexandra and Bohrer, Gil and Miller, Christopher S. and Wrighton, Kelly C. and Orsi, William},
abstractNote = {Wetland soils are one of the largest natural contributors to the emission of methane, a potent greenhouse gas. Currently, microbial contributions to methane emissions from these systems emphasize the roles of acetoclastic and hydrogenotrophic methanogens, while less frequently considering methyl-group substrates (e.g., methanol and methylamines). Here, we integrated laboratory and field experiments to explore the potential for methylotrophic methanogenesis in Old Woman Creek (OWC), a temperate freshwater wetland located in Ohio, USA. We first demonstrated the capacity for methylotrophic methanogenesis in these soils using laboratory soil microcosms amended with trimethylamine. However, subsequent field porewater nuclear magnetic resonance (NMR) analyses to identify methanogenic substrates failed to detect evidence for methylamine compounds in soil porewaters, instead noting the presence of the methylotrophic substrate methanol. Accordingly, our wetland soil-derived metatranscriptomic data indicated that methanol utilization by theMethanomassiliicoccaceaewas the likely source of methylotrophic methanogenesis.Methanomassiliicoccaceaerelative contributions tomcrAtranscripts nearly doubled with depth, accounting for up to 8% of themcrAtranscripts in 25-cm-deep soils. Longitudinal 16S rRNA amplicon andmcrAgene surveys demonstrated thatMethanomassiliicoccaceaewere stably present over 2 years across lateral and depth gradients in this wetland. Meta-analysis of 16S rRNA sequences similar (>99%) to OWCMethanomassiliicoccaceaein public databases revealed a global distribution, with a high representation in terrestrial soils and sediments. Together, our results demonstrate that methylotrophic methanogenesis likely contributes to methane flux from climatically relevant wetland soils. IMPORTANCEUnderstanding the sources and controls on microbial methane production from wetland soils is critical to global methane emission predictions, particularly in light of changing climatic conditions. Current biogeochemical models of methanogenesis consider only acetoclastic and hydrogenotrophic sources and exclude methylotrophic methanogenesis, potentially underestimating microbial contributions to methane flux. Our multi-omic results demonstrated that methylotrophic methanogens of the familyMethanomassiliicoccaceaewere present and active in a freshwater wetland, with metatranscripts indicating that methanol, not methylamines, was the likely substrate under the conditions measured here. However, laboratory experiments indicated the potential for other methanogens to become enriched in response to trimethylamine, revealing the reservoir of methylotrophic methanogenesis potential residing in these soils. Collectively, our approach used coupled field and laboratory investigations to illuminate metabolisms influencing the terrestrial microbial methane cycle, thereby offering direction for increased realism in predictive process-oriented models of methane flux in wetland soils.},
doi = {10.1128/msystems.00320-19},
journal = {mSystems},
number = 6,
volume = 4,
place = {United States},
year = {2019},
month = {12}
}

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