DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils

Abstract

The availability of labile carbon (C) compounds in Arctic wetland soils is expected to increase due to thawing permafrost and increased fermentation as a result of decomposition of organic matter with warming. How microbial communities respond to this change will affect the balance of CO2 and CH4 emitted during anaerobic organic matter decomposition, and ultimately the net radiative forcing of greenhouse gas emissions from these soils. While soil water content limits aerobic respiration, the factors controlling methanogenesis and anaerobic respiration are poorly defined in suboxic Arctic soils. In this study, we conducted incubation experiments on two tundra soils from field sites on the Seward Peninsula, Alaska, with contrasting pH and geochemistry to determine the pathways of anaerobic microbial respiration and changes with increasing substrate availability upon warming. In incubation of soils from the circumneutral Teller site, the ratio of CO2 to CH4 dropped from 10 to <2 after 60 days, indicating rapid depletion of alternative terminal electron acceptors (TEAs). Addition of acetate stimulated production of CO2 and CH4 in a nearly 1:1 ratio, consistent with methanogenesis, and the composition of the microbial community shifted to favor clades capable of utilizing the added acetate such as the Fe(III)-reducing Geobacter and themore » methanogenic archaea Methanosarcina. In contrast, both CO2 and CH4 production declined with acetate addition during incubation of soils from the more acidic Council site, and fermentative microorganisms increased in abundance despite the high availability of fermentation products. These results demonstrate that the degree to which increasing substrate availability stimulates greenhouse gas production in tundra wetlands will vary widely depending on soil pH and geochemistry.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Hope College, Holland, MI (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Oakland Univ., Rochester, MI (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
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:
1661241
Alternate Identifier(s):
OSTI ID: 1658423
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Science: Processes & Impacts
Additional Journal Information:
Journal Volume: 22; Journal Issue: 9; Journal ID: ISSN 2050-7887
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Philben, Michael J., Zhang, Lijie, Yang, Ziming, Taş, Neslihan, Wullschleger, Stan D., Graham, David E., and Gu, Baohua. Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils. United States: N. p., 2020. Web. doi:10.1039/d0em00124d.
Philben, Michael J., Zhang, Lijie, Yang, Ziming, Taş, Neslihan, Wullschleger, Stan D., Graham, David E., & Gu, Baohua. Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils. United States. https://doi.org/10.1039/d0em00124d
Philben, Michael J., Zhang, Lijie, Yang, Ziming, Taş, Neslihan, Wullschleger, Stan D., Graham, David E., and Gu, Baohua. Fri . "Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils". United States. https://doi.org/10.1039/d0em00124d. https://www.osti.gov/servlets/purl/1661241.
@article{osti_1661241,
title = {Anaerobic respiration pathways and response to increased substrate availability of Arctic wetland soils},
author = {Philben, Michael J. and Zhang, Lijie and Yang, Ziming and Taş, Neslihan and Wullschleger, Stan D. and Graham, David E. and Gu, Baohua},
abstractNote = {The availability of labile carbon (C) compounds in Arctic wetland soils is expected to increase due to thawing permafrost and increased fermentation as a result of decomposition of organic matter with warming. How microbial communities respond to this change will affect the balance of CO2 and CH4 emitted during anaerobic organic matter decomposition, and ultimately the net radiative forcing of greenhouse gas emissions from these soils. While soil water content limits aerobic respiration, the factors controlling methanogenesis and anaerobic respiration are poorly defined in suboxic Arctic soils. In this study, we conducted incubation experiments on two tundra soils from field sites on the Seward Peninsula, Alaska, with contrasting pH and geochemistry to determine the pathways of anaerobic microbial respiration and changes with increasing substrate availability upon warming. In incubation of soils from the circumneutral Teller site, the ratio of CO2 to CH4 dropped from 10 to <2 after 60 days, indicating rapid depletion of alternative terminal electron acceptors (TEAs). Addition of acetate stimulated production of CO2 and CH4 in a nearly 1:1 ratio, consistent with methanogenesis, and the composition of the microbial community shifted to favor clades capable of utilizing the added acetate such as the Fe(III)-reducing Geobacter and the methanogenic archaea Methanosarcina. In contrast, both CO2 and CH4 production declined with acetate addition during incubation of soils from the more acidic Council site, and fermentative microorganisms increased in abundance despite the high availability of fermentation products. These results demonstrate that the degree to which increasing substrate availability stimulates greenhouse gas production in tundra wetlands will vary widely depending on soil pH and geochemistry.},
doi = {10.1039/d0em00124d},
journal = {Environmental Science: Processes & Impacts},
number = 9,
volume = 22,
place = {United States},
year = {Fri Aug 28 00:00:00 EDT 2020},
month = {Fri Aug 28 00:00:00 EDT 2020}
}

Works referenced in this record:

Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri
journal, May 2014

  • Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua
  • Applied and Environmental Microbiology, Vol. 80, Issue 15
  • DOI: 10.1128/AEM.00895-14

The specificity of growth inhibition of methanogenic bacteria by bromoethanesulfonate
journal, December 1987

  • Sparling, Richard; Daniels, Lacy
  • Canadian Journal of Microbiology, Vol. 33, Issue 12
  • DOI: 10.1139/m87-199

Methane fluxes in the high northern latitudes for 2005–2013 estimated using a Bayesian atmospheric inversion
journal, January 2017

  • Thompson, Rona L.; Sasakawa, Motoki; Machida, Toshinobu
  • Atmospheric Chemistry and Physics, Vol. 17, Issue 5
  • DOI: 10.5194/acp-17-3553-2017

Modeling anaerobic soil organic carbon decomposition in Arctic polygon tundra: insights into soil geochemical influences on carbon mineralization
journal, January 2019

  • Zheng, Jianqiu; Thornton, Peter E.; Painter, Scott L.
  • Biogeosciences, Vol. 16, Issue 3
  • DOI: 10.5194/bg-16-663-2019

Climate change and the permafrost carbon feedback
journal, April 2015

  • Schuur, E. A. G.; McGuire, A. D.; Schädel, C.
  • Nature, Vol. 520, Issue 7546
  • DOI: 10.1038/nature14338

Characterization of iron oxide nanoparticle films at the air–water interface in Arctic tundra waters
journal, August 2018


Organic-matter quality of deep permafrost carbon – a study from Arctic Siberia
journal, January 2015


Compilation of Henry's law constants (version 4.0) for water as solvent
journal, January 2015


Adsorption of Sulfate by Kaolinite and Amorphous Iron Oxide in the Presence of Organic Ligands
journal, July 1989


An Ordination of the Upland Forest Communities of Southern Wisconsin
journal, February 1957

  • Bray, J. Roger; Curtis, J. T.
  • Ecological Monographs, Vol. 27, Issue 4
  • DOI: 10.2307/1942268

Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
journal, December 2012

  • Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
  • Nature Methods, Vol. 10, Issue 1
  • DOI: 10.1038/nmeth.2276

Intracellular pH of acid-tolerant ruminal bacteria.
journal, January 1991


Stimulation of anaerobic organic matter decomposition by subsurface organic N addition in tundra soils
journal, March 2019


Ecosystem and physiological controls over methane production in northern wetlands
journal, January 1994

  • Valentine, David W.; Holland, Elisabeth A.; Schimel, David S.
  • Journal of Geophysical Research, Vol. 99, Issue D1
  • DOI: 10.1029/93JD00391

Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Interaction of Carbonate and Organic Anions with Sulfate and Selenate Adsorption on an Aluminum Oxide
journal, May 2000


Stable carbon isotope fractionation during methanogenesis in three boreal peatland ecosystems
journal, January 2010


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Reduction of iron (III) and humic substances plays a major role in anaerobic respiration in an Arctic peat soil
journal, January 2010

  • Lipson, David A.; Jha, Mony; Raab, Theodore K.
  • Journal of Geophysical Research, Vol. 115
  • DOI: 10.1029/2009JG001147

Biogeochemical modeling of CO 2 and CH 4 production in anoxic Arctic soil microcosms
journal, January 2016


Trophic links between fermenters and methanogens in a moderately acidic fen soil
journal, June 2009


FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


The effect of permafrost thaw on old carbon release and net carbon exchange from tundra
journal, May 2009

  • Schuur, Edward A. G.; Vogel, Jason G.; Crummer, Kathryn G.
  • Nature, Vol. 459, Issue 7246
  • DOI: 10.1038/nature08031

Pathways of anaerobic organic matter decomposition in tundra soils from Barrow, Alaska: BIOGEOCHEMISTRY OF ANOXIC ARCTIC TUNDRA
journal, November 2015

  • Herndon, Elizabeth M.; Mann, Benjamin F.; Roy Chowdhury, Taniya
  • Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 11
  • DOI: 10.1002/2015JG003147

Hydrogenotrophic Methanogenesis by Moderately Acid-Tolerant Methanogens of a Methane-Emitting Acidic Peat
journal, January 2003


phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Selective Inhibition by 2-Bromoethanesulfonate of Methanogenesis from Acetate in a Thermophilic Anaerobic Digestor
journal, January 1984


UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013


Anaerobic microbial biogeochemistry in a northern bog: Acetate as a dominant metabolic end product: ANAEROBIC MICROBIAL BIOGEOCHEMISTRY IN A NORTHERN BOG
journal, October 2002

  • Duddleston, Khrystyne N.; Kinney, Monica A.; Kiene, Ronald P.
  • Global Biogeochemical Cycles, Vol. 16, Issue 4
  • DOI: 10.1029/2001GB001402

Redox properties of standard humic acids
journal, August 2001


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp.
journal, June 1992


Methane suppression by iron and humic acids in soils of the Arctic Coastal Plain
journal, April 2015


Biogenic volatile release from permafrost thaw is determined by the soil microbial sink
journal, August 2018


The thermodynamic ladder in geomicrobiology
journal, March 2011

  • Bethke, C. M.; Sanford, R. A.; Kirk, M. F.
  • American Journal of Science, Vol. 311, Issue 3
  • DOI: 10.2475/03.2011.01

Stimulation of Methanogenesis by Slurries of Saltmarsh Sediment after the Addition of Molybdate to Inhibit Sulphate-reducing Bacteria
journal, January 1983


Humics as an electron donor for anaerobic respiration
journal, February 1999


Geochemical drivers of organic matter decomposition in arctic tundra soils
journal, December 2015


Arctic Soil Governs Whether Climate Change Drives Global Losses or Gains in Soil Carbon
journal, December 2019

  • Wieder, William R.; Sulman, Benjamin N.; Hartman, Melannie D.
  • Geophysical Research Letters, Vol. 46, Issue 24
  • DOI: 10.1029/2019GL085543

Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation
journal, January 2012

  • McCarthy, Davis J.; Chen, Yunshun; Smyth, Gordon K.
  • Nucleic Acids Research, Vol. 40, Issue 10
  • DOI: 10.1093/nar/gks042

Solid-phase organic matter reduction regulates anaerobic decomposition in bog soil
journal, May 2013


Bacterial community structure and soil properties of a subarctic tundra soil in Council, Alaska
journal, August 2014

  • Kim, Hye Min; Jung, Ji Young; Yergeau, Etienne
  • FEMS Microbiology Ecology, Vol. 89, Issue 2
  • DOI: 10.1111/1574-6941.12362

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

A Membrane-Bound Cytochrome Enables Methanosarcina acetivorans To Conserve Energy from Extracellular Electron Transfer
journal, August 2019


Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales
journal, February 2013

  • Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K.
  • Global Change Biology, Vol. 19, Issue 5
  • DOI: 10.1111/gcb.12131

Humic acids as electron acceptors in wetland decomposition
journal, July 2009

  • Keller, Jason K.; Weisenhorn, Pamela B.; Megonigal, J. Patrick
  • Soil Biology and Biochemistry, Vol. 41, Issue 7
  • DOI: 10.1016/j.soilbio.2009.04.008

Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil
journal, April 2016


Ancient low–molecular-weight organic acids in permafrost fuel rapid carbon dioxide production upon thaw
journal, October 2015

  • Drake, Travis W.; Wickland, Kimberly P.; Spencer, Robert G. M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 45
  • DOI: 10.1073/pnas.1511705112

Different Temperature Optima for Methane Formation When Enrichments from Acid Peat Are Supplemented with Acetate or Hydrogen
journal, January 1984


Electron Donors Utilized by Sulfate-Reducing Bacteria in Eutrophic Lake Sediments †
journal, January 1981


Hydrogenation of organic matter as a terminal electron sink sustains high CO2:CH4 production ratios during anaerobic decomposition
journal, October 2017


Syntrophic Acetate-Oxidizing Microbes in Methanogenic Environments
journal, January 2008


Transport, anoxia and end-product accumulation control carbon dioxide and methane production and release in peat soils
journal, March 2017