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Title: Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States)

Abstract

Climate warming is predicted to increase heterotrophic metabolism in northern peatland soils leading to enhanced greenhouse gas emissions. However, the specific relationships between temperature and the greenhouse gas producing microbial communities are poorly understood. Thus, in this study, the temperature dependence of carbon dioxide (CO2) and methane (CH4) production rates along with abundance and composition of microbial communities were investigated in peat from a Sphagnum-dominated peatland, S1 bog (Minnesota, United States). Whereas CH4 production rates increased with temperature up to 30°C, CO2 production did not, resulting in a lower CO2:CH4 ratio with increasing temperature. CO2 production showed both psychrophilic and mesophilic maxima at 4 and 20°C, respectively, and appears to be mediated by two anaerobic microbial communities, one that operates under psychrophilic conditions that predominate for much of the year, and another that is more active under warmer conditions during the growing season. In incubations at 10°C above the ambient range, members of the Clostridiaceae and hydrogenotrophic methanogens of the Methanobacteriaceae dominated. Moreover, a significant negative correlation between temperature and microbial diversity was observed. Results indicate that the potential consequences of warming surface peat in northern peatlands include a large stimulation in CH4 production and a significant loss of microbialmore » diversity.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Georgia Institute of Technology, Atlanta, GA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1509497
Alternate Identifier(s):
OSTI ID: 1610942
Grant/Contract Number:  
SC0007144; SC0012088
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 10; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; peatlands; climate change; methanogenesis; microbial community; microbial diversity

Citation Formats

Kolton, Max, Marks, Ansley, Wilson, Rachel M., Chanton, Jeffrey P., and Kostka, Joel E. Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States). Switzerland: N. p., 2019. Web. doi:10.3389/fmicb.2019.00870.
Kolton, Max, Marks, Ansley, Wilson, Rachel M., Chanton, Jeffrey P., & Kostka, Joel E. Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States). Switzerland. https://doi.org/10.3389/fmicb.2019.00870
Kolton, Max, Marks, Ansley, Wilson, Rachel M., Chanton, Jeffrey P., and Kostka, Joel E. Fri . "Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States)". Switzerland. https://doi.org/10.3389/fmicb.2019.00870.
@article{osti_1509497,
title = {Impact of Warming on Greenhouse Gas Production and Microbial Diversity in Anoxic Peat From a Sphagnum-Dominated Bog (Grand Rapids, Minnesota, United States)},
author = {Kolton, Max and Marks, Ansley and Wilson, Rachel M. and Chanton, Jeffrey P. and Kostka, Joel E.},
abstractNote = {Climate warming is predicted to increase heterotrophic metabolism in northern peatland soils leading to enhanced greenhouse gas emissions. However, the specific relationships between temperature and the greenhouse gas producing microbial communities are poorly understood. Thus, in this study, the temperature dependence of carbon dioxide (CO2) and methane (CH4) production rates along with abundance and composition of microbial communities were investigated in peat from a Sphagnum-dominated peatland, S1 bog (Minnesota, United States). Whereas CH4 production rates increased with temperature up to 30°C, CO2 production did not, resulting in a lower CO2:CH4 ratio with increasing temperature. CO2 production showed both psychrophilic and mesophilic maxima at 4 and 20°C, respectively, and appears to be mediated by two anaerobic microbial communities, one that operates under psychrophilic conditions that predominate for much of the year, and another that is more active under warmer conditions during the growing season. In incubations at 10°C above the ambient range, members of the Clostridiaceae and hydrogenotrophic methanogens of the Methanobacteriaceae dominated. Moreover, a significant negative correlation between temperature and microbial diversity was observed. Results indicate that the potential consequences of warming surface peat in northern peatlands include a large stimulation in CH4 production and a significant loss of microbial diversity.},
doi = {10.3389/fmicb.2019.00870},
journal = {Frontiers in Microbiology},
number = ,
volume = 10,
place = {Switzerland},
year = {Fri Apr 26 00:00:00 EDT 2019},
month = {Fri Apr 26 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fmicb.2019.00870

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Cited by: 35 works
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Works referenced in this record:

Small differences in ombrotrophy control regional-scale variation in methane cycling among Sphagnum-dominated peatlands
journal, June 2018


Effects of experimental warming on biodiversity depend on ecosystem type and local species composition
journal, September 2016

  • Gruner, Daniel S.; Bracken, Matthew E. S.; Berger, Stella A.
  • Oikos, Vol. 126, Issue 1
  • DOI: 10.1111/oik.03688

Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO 2 atmosphere
journal, January 2017

  • Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert
  • Biogeosciences, Vol. 14, Issue 4
  • DOI: 10.5194/bg-14-861-2017

Clostridium ultunense sp. nov., a Mesophilic Bacterium Oxidizing Acetate in Syntrophic Association with a Hydrogenotrophic Methanogenic Bacterium
journal, October 1996

  • Schnurer, A.; Schink, B.; Svensson, B. H.
  • International Journal of Systematic Bacteriology, Vol. 46, Issue 4
  • DOI: 10.1099/00207713-46-4-1145

Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
journal, January 1993


Stability of peatland carbon to rising temperatures
journal, December 2016

  • Wilson, R. M.; Hopple, A. M.; Tfaily, M. M.
  • Nature Communications, Vol. 7, Article No. 13723
  • DOI: 10.1038/ncomms13723

A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning
journal, September 2011


Northern Peatlands: Role in the Carbon Cycle and Probable Responses to Climatic Warming
journal, May 1991

  • Gorham, Eville
  • Ecological Applications, Vol. 1, Issue 2
  • DOI: 10.2307/1941811

Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions
journal, November 2017


Reconstructing the Microbial Diversity and Function of Pre-Agricultural Tallgrass Prairie Soils in the United States
journal, October 2013


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


Temperature sensitivity of peatland C and N cycling: Does substrate supply play a role?
journal, June 2013


Moving Beyond Global Warming Potentials to Quantify the Climatic Role of Ecosystems
journal, May 2015


Microbial Metabolic Potential for Carbon Degradation and Nutrient (Nitrogen and Phosphorus) Acquisition in an Ombrotrophic Peatland
journal, March 2014

  • Lin, Xueju; Tfaily, Malak M.; Green, Stefan J.
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/AEM.00206-14

Global atmospheric methane: budget, changes and dangers
journal, May 2011

  • Dlugokencky, Edward J.; Nisbet, Euan G.; Fisher, Rebecca
  • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 369, Issue 1943
  • DOI: 10.1098/rsta.2010.0341

Soil biodiversity and soil community composition determine ecosystem multifunctionality
journal, March 2014

  • Wagg, C.; Bender, S. F.; Widmer, F.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
  • DOI: 10.1073/pnas.1320054111

Microbial Community Structure and Activity Linked to Contrasting Biogeochemical Gradients in Bog and Fen Environments of the Glacial Lake Agassiz Peatland
journal, July 2012

  • Lin, X.; Green, S.; Tfaily, M. M.
  • Applied and Environmental Microbiology, Vol. 78, Issue 19
  • DOI: 10.1128/AEM.01750-12

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


Methane production and consumption in temperate and subarctic peat soils: Response to temperature and pH
journal, March 1993


Evidence for methane production by saprotrophic fungi
journal, January 2012

  • Lenhart, Katharina; Bunge, Michael; Ratering, Stefan
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms2049

Microbial communities and their relevance for ecosystem models: Decomposition as a case study
journal, April 2010


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

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

Methanogenic Pathway and Archaeal Community Structure in the Sediment of Eutrophic Lake Dagow: Effect of Temperature
journal, June 2004


Differential abundance analysis for microbial marker-gene surveys
journal, September 2013

  • Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
  • Nature Methods, Vol. 10, Issue 12
  • DOI: 10.1038/nmeth.2658

Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature
journal, December 2001


Intermediary ecosystem metabolism as a main driver of methanogenesis in acidic wetland soil: Drivers of methanogenesis in fen soil
journal, July 2009


Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association
journal, May 2016

  • Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta
  • Genome Biology and Evolution, Vol. 8, Issue 6
  • DOI: 10.1093/gbe/evw114

grofit : Fitting Biological Growth Curves with R
journal, January 2010

  • Kahm, Matthias; Hasenbrink, Guido; Lichtenberg-Fraté, Hella
  • Journal of Statistical Software, Vol. 33, Issue 7
  • DOI: 10.18637/jss.v033.i07

Methane fluxes show consistent temperature dependence across microbial to ecosystem scales
journal, March 2014

  • Yvon-Durocher, Gabriel; Allen, Andrew P.; Bastviken, David
  • Nature, Vol. 507, Issue 7493
  • DOI: 10.1038/nature13164

Microbial diversity drives multifunctionality in terrestrial ecosystems
journal, January 2016

  • Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Reich, Peter B.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10541

Phylogenomic Data Support a Seventh Order of Methylotrophic Methanogens and Provide Insights into the Evolution of Methanogenesis
journal, August 2013

  • Borrel, Guillaume; O’Toole, Paul W.; Harris, Hugh M. B.
  • Genome Biology and Evolution, Vol. 5, Issue 10
  • DOI: 10.1093/gbe/evt128

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


Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
journal, April 2015

  • Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 19
  • DOI: 10.1073/pnas.1420797112

Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS
journal, June 2009

  • Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G.
  • Global Biogeochemical Cycles, Vol. 23, Issue 2
  • DOI: 10.1029/2008GB003327

Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011


Response of Methanogens in Arctic Sediments to Temperature and Methanogenic Substrate Availability
journal, June 2015


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

Peatland types influence the inhibitory effects of a humic substance analog on methane production
journal, March 2016


Responses of methanogenic and methanotrophic communities to warming in varying moisture regimes of two boreal fens
journal, June 2016


Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO 2 /CH 4 Production Ratios
journal, December 2016

  • Juottonen, Heli; Eiler, Alexander; Biasi, Christina
  • Applied and Environmental Microbiology, Vol. 83, Issue 4
  • DOI: 10.1128/AEM.02533-16

Biochar-stimulated plant performance is strongly linked to microbial diversity and metabolic potential in the rhizosphere
journal, October 2016

  • Kolton, Max; Graber, Ellen R.; Tsehansky, Ludmila
  • New Phytologist, Vol. 213, Issue 3
  • DOI: 10.1111/nph.14253

Microbial Community Stratification Linked to Utilization of Carbohydrates and Phosphorus Limitation in a Boreal Peatland at Marcell Experimental Forest, Minnesota, USA
journal, March 2014

  • Lin, Xueju; Tfaily, Malak M.; Steinweg, J. Megan
  • Applied and Environmental Microbiology, Vol. 80, Issue 11
  • DOI: 10.1128/AEM.00205-14

A pan-Arctic synthesis of CH 4 and CO 2 production from anoxic soil incubations
journal, March 2015

  • Treat, Claire C.; Natali, Susan M.; Ernakovich, Jessica
  • Global Change Biology, Vol. 21, Issue 7
  • DOI: 10.1111/gcb.12875

Thermal deactivation of high-affinity H2 uptake activity in soils
journal, September 2010


Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production
journal, April 2014

  • Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
  • DOI: 10.1073/pnas.1314641111

Comparison of temperature effects on soil respiration and bacterial and fungal growth rates
journal, March 2005

  • PietikÃ¥inen, Janna; Pettersson, Marie; Bååth, Erland
  • FEMS Microbiology Ecology, Vol. 52, Issue 1
  • DOI: 10.1016/j.femsec.2004.10.002

Pathways of anaerobic carbon cycling across an ombrotrophic-minerotrophic peatland gradient
journal, January 2007


Microbes and global carbon
journal, September 2013


Influence of temperature and high acetate concentrations on methanogenensis in lake sediment slurries: Temperature influence on methanogenesis in lake sediment
journal, December 2007


Methanogenesis and methanogenic pathways in a peat from subarctic permafrost
journal, April 2007


Conservation evaluation and phylogenetic diversity
journal, January 1992


Can Sphagnum leachate chemistry explain differences in anaerobic decomposition in peatlands?
journal, July 2015


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


Rate of warming affects temperature sensitivity of anaerobic peat decomposition and greenhouse gas production
journal, September 2017

  • Sihi, Debjani; Inglett, Patrick W.; Gerber, Stefan
  • Global Change Biology, Vol. 24, Issue 1
  • DOI: 10.1111/gcb.13839

Molybdenum-Based Diazotrophy in a Sphagnum Peatland in Northern Minnesota
journal, June 2017

  • Warren, Melissa J.; Lin, Xueju; Gaby, John C.
  • Applied and Environmental Microbiology, Vol. 83, Issue 17
  • DOI: 10.1128/AEM.01174-17

Homoacetogenesis: A potentially underappreciated carbon pathway in peatlands
journal, January 2014


Effects of temperature on the diversity and community structure of known methanogenic groups and other archaea in high Arctic peat
journal, November 2007

  • Høj, Lone; Olsen, Rolf A.; Torsvik, Vigdis L.
  • The ISME Journal, Vol. 2, Issue 1
  • DOI: 10.1038/ismej.2007.84

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

Global soil carbon projections are improved by modelling microbial processes
journal, July 2013

  • Wieder, William R.; Bonan, Gordon B.; Allison, Steven D.
  • Nature Climate Change, Vol. 3, Issue 10
  • DOI: 10.1038/nclimate1951

Temperature sensitivity of soil carbon decomposition and feedbacks to climate change
journal, March 2006


Niche and metabolic principles explain patterns of diversity and distribution: theory and a case study with soil bacterial communities
journal, June 2015

  • Okie, Jordan G.; Van Horn, David J.; Storch, David
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1809
  • DOI: 10.1098/rspb.2014.2630

Archaea in Biogeochemical Cycles
journal, September 2013


Humic substances as fully regenerable electron acceptors in recurrently anoxic environments
journal, February 2014

  • Klüpfel, Laura; Piepenbrock, Annette; Kappler, Andreas
  • Nature Geoscience, Vol. 7, Issue 3
  • DOI: 10.1038/ngeo2084

Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming
journal, May 2018

  • Alvarez, Gaël; Shahzad, Tanvir; Andanson, Laurence
  • Global Change Biology, Vol. 24, Issue 9
  • DOI: 10.1111/gcb.14281

Reconciling the temperature dependence of respiration across timescales and ecosystem types
journal, June 2012

  • Yvon-Durocher, Gabriel; Caffrey, Jane M.; Cescatti, Alessandro
  • Nature, Vol. 487, Issue 7408
  • DOI: 10.1038/nature11205

Correlation of Methane Production and Functional Gene Transcriptional Activity in a Peat Soil
journal, September 2009

  • Freitag, T. E.; Prosser, J. I.
  • Applied and Environmental Microbiology, Vol. 75, Issue 21
  • DOI: 10.1128/AEM.01021-09

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


Anaerobic trophic interactions of contrasting methane-emitting mire soils: processes versus taxa
journal, April 2015

  • Hunger, Sindy; Gößner, Anita S.; Drake, Harold L.
  • FEMS Microbiology Ecology, Vol. 91, Issue 5
  • DOI: 10.1093/femsec/fiv045

Temperature impacts differentially on the methanogenic food web of cellulose-supplemented peatland soil: Differential temperature effects on peat microbes
journal, June 2014

  • Schmidt, Oliver; Horn, Marcus A.; Kolb, Steffen
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12507

Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008

  • Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
  • Nature Reviews Microbiology, Vol. 6, Issue 8
  • DOI: 10.1038/nrmicro1931

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

Soil-carbon response to warming dependent on microbial physiology
journal, April 2010

  • Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A.
  • Nature Geoscience, Vol. 3, Issue 5
  • DOI: 10.1038/ngeo846

Denitrification in salt marsh sediments: Evidence for seasonal temperature selection among populations of denitrifiers
journal, September 1977

  • Kaplan, Warren A.; Teal, John M.; Valiela, Ivan
  • Microbial Ecology, Vol. 3, Issue 3
  • DOI: 10.1007/BF02010617

Diversity is the question, not the answer
journal, September 2016


Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction
journal, January 2005

  • Yu, Youngseob; Lee, Changsoo; Kim, Jaai
  • Biotechnology and Bioengineering, Vol. 89, Issue 6
  • DOI: 10.1002/bit.20347

Alpha- and Gammaproteobacterial Methanotrophs Codominate the Active Methane-Oxidizing Communities in an Acidic Boreal Peat Bog
journal, February 2016

  • Esson, Kaitlin C.; Lin, Xueju; Kumaresan, Deepak
  • Applied and Environmental Microbiology, Vol. 82, Issue 8
  • DOI: 10.1128/AEM.03640-15

Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839