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

Title: Sequential Abiotic-Biotic Processes Drive Organic Carbon Transformation in Peat Bogs

Abstract

Abstract Peatlands, which store one third of the terrestrial carbon (C), are subject to large disturbances under a changing climate. It is crucial to understand how microbial and physiochemical factors affect the vulnerability of these large C stores to predict climate‐induced greenhouse gas fluxes. Here, we used a combination of mass spectrometry and spectroscopy techniques, to understand sequential biotic and abiotic degradation pathways of Sphagnum fallax leachate in an anaerobic incubation experiment, in the presence and absence of microorganisms. Removal of microorganisms was carried out by passing aqueous samples through 0.2‐µm filters. Our results revealed that S. fallax leachate degradation by abiotic reactions is a significant contributor to CO 2 production. Further, abiotic factors, such as low pH, are responsible for partial dissolved organic carbon (DOC) degradation that produces bioavailable compounds that shift microbial metabolic pathways and stimulate respiration in peat bogs. Acid‐catalyzed hydrolysis of Sphagnum ‐ produced glycosides can provide the microbial communities with glucose and stimulate microbial respiration of DOC to CO 2 . These results, while unique to peatlands, demonstrate the importance and underscore the complexity of sequential abiotic and biotic processes on C cycling in peat bogs. It is therefore crucial to incorporate abiotic degradation andmore » sequential below‐ground biotic and abiotic interactions into climate models for a better prediction of the influence of climate change on DOC stability in peatlands. These findings might not be representative of other ecosystems with different environmental conditions including mineral‐rich peatlands and plant matter in surface peat horizons that comprise discrete microbial populations, and DOC composition.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2]; ORCiD logo [3];  [2]; ORCiD logo [2]; ORCiD logo [4]; ORCiD logo [1]; ORCiD logo [5]; ORCiD logo [6]
  1. Univ. of Arizona, Tucson, AZ (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Bruker Daltonics Inc., Billercia, MA (United States)
  4. Department of Environmental Science The University of Arizona Tucson AZ USA
  5. Florida State Univ., Tallahassee, FL (United States)
  6. Univ. of Arizona, Tucson, AZ (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE Office of Science (SC)
OSTI Identifier:
1781660
Alternate Identifier(s):
OSTI ID: 1786687
Report Number(s):
PNNL-SA-160453
Journal ID: ISSN 2169-8953
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Geophysical Research. Biogeosciences
Additional Journal Information:
Journal Volume: 126; Journal Issue: 2; Journal ID: ISSN 2169-8953
Publisher:
American Geophysical Union
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; abiotic; biotic; degradation pathways; mass spectrometry; metabolites; peat bogs

Citation Formats

Fudyma, Jane D., Toyoda, Jason G., Chu, Rosalie K., Weitz, Karl K., Heyman, Heino M., Eder, Elizabeth, Hoyt, David W., Gieschen, Hans, Graf Grachet, Nathalia, Wilson, Rachel M., and Tfaily, Malak M. Sequential Abiotic-Biotic Processes Drive Organic Carbon Transformation in Peat Bogs. United States: N. p., 2021. Web. doi:10.1029/2020jg006079.
Fudyma, Jane D., Toyoda, Jason G., Chu, Rosalie K., Weitz, Karl K., Heyman, Heino M., Eder, Elizabeth, Hoyt, David W., Gieschen, Hans, Graf Grachet, Nathalia, Wilson, Rachel M., & Tfaily, Malak M. Sequential Abiotic-Biotic Processes Drive Organic Carbon Transformation in Peat Bogs. United States. https://doi.org/10.1029/2020jg006079
Fudyma, Jane D., Toyoda, Jason G., Chu, Rosalie K., Weitz, Karl K., Heyman, Heino M., Eder, Elizabeth, Hoyt, David W., Gieschen, Hans, Graf Grachet, Nathalia, Wilson, Rachel M., and Tfaily, Malak M. Fri . "Sequential Abiotic-Biotic Processes Drive Organic Carbon Transformation in Peat Bogs". United States. https://doi.org/10.1029/2020jg006079. https://www.osti.gov/servlets/purl/1781660.
@article{osti_1781660,
title = {Sequential Abiotic-Biotic Processes Drive Organic Carbon Transformation in Peat Bogs},
author = {Fudyma, Jane D. and Toyoda, Jason G. and Chu, Rosalie K. and Weitz, Karl K. and Heyman, Heino M. and Eder, Elizabeth and Hoyt, David W. and Gieschen, Hans and Graf Grachet, Nathalia and Wilson, Rachel M. and Tfaily, Malak M.},
abstractNote = {Abstract Peatlands, which store one third of the terrestrial carbon (C), are subject to large disturbances under a changing climate. It is crucial to understand how microbial and physiochemical factors affect the vulnerability of these large C stores to predict climate‐induced greenhouse gas fluxes. Here, we used a combination of mass spectrometry and spectroscopy techniques, to understand sequential biotic and abiotic degradation pathways of Sphagnum fallax leachate in an anaerobic incubation experiment, in the presence and absence of microorganisms. Removal of microorganisms was carried out by passing aqueous samples through 0.2‐µm filters. Our results revealed that S. fallax leachate degradation by abiotic reactions is a significant contributor to CO 2 production. Further, abiotic factors, such as low pH, are responsible for partial dissolved organic carbon (DOC) degradation that produces bioavailable compounds that shift microbial metabolic pathways and stimulate respiration in peat bogs. Acid‐catalyzed hydrolysis of Sphagnum ‐ produced glycosides can provide the microbial communities with glucose and stimulate microbial respiration of DOC to CO 2 . These results, while unique to peatlands, demonstrate the importance and underscore the complexity of sequential abiotic and biotic processes on C cycling in peat bogs. It is therefore crucial to incorporate abiotic degradation and sequential below‐ground biotic and abiotic interactions into climate models for a better prediction of the influence of climate change on DOC stability in peatlands. These findings might not be representative of other ecosystems with different environmental conditions including mineral‐rich peatlands and plant matter in surface peat horizons that comprise discrete microbial populations, and DOC composition.},
doi = {10.1029/2020jg006079},
journal = {Journal of Geophysical Research. Biogeosciences},
number = 2,
volume = 126,
place = {United States},
year = {Fri Jan 29 00:00:00 EST 2021},
month = {Fri Jan 29 00:00:00 EST 2021}
}

Works referenced in this record:

Antibacterial activity of sphagnum acid and other phenolic compounds found in Sphagnum papillosum against food-borne bacteria
journal, July 2009


The ecological significance of organochemical compounds in Sphagnum
journal, June 1997


Vulnerability of Permafrost Carbon to Climate Change: Implications for the Global Carbon Cycle
journal, September 2008

  • Schuur, Edward A. G.; Bockheim, James; Canadell, Josep G.
  • BioScience, Vol. 58, Issue 8
  • DOI: 10.1641/B580807

Plant species traits are the predominant control on litter decomposition rates within biomes worldwide
journal, October 2008


Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra
journal, November 2017


Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw
journal, August 2020

  • Hugelius, Gustaf; Loisel, Julie; Chadburn, Sarah
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 34
  • DOI: 10.1073/pnas.1916387117

Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling
journal, November 1992


Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms
journal, April 2015


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

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

Kinetic Study on the Acid-Catalyzed Hydrolysis of Cellulose to Levulinic Acid
journal, March 2007

  • Girisuta, B.; Janssen, L. P. B. M.; Heeres, H. J.
  • Industrial & Engineering Chemistry Research, Vol. 46, Issue 6
  • DOI: 10.1021/ie061186z

Peculiarities of the composition of acids in Sphagnum species of the percolation bog of the Kolkheti lowland
journal, June 2018

  • Tetemadze, Natela; Bakuridze, Alyosha; Jokhadze, Malkhaz
  • Annals of Agrarian Science, Vol. 16, Issue 2
  • DOI: 10.1016/j.aasci.2018.04.012

pH as a Primary Control in Environmental Microbiology: 1. Thermodynamic Perspective
journal, May 2018


The Sphagnum microbiome: new insights from an ancient plant lineage
journal, February 2016

  • Kostka, Joel E.; Weston, David J.; Glass, Jennifer B.
  • New Phytologist, Vol. 211, Issue 1
  • DOI: 10.1111/nph.13993

Surface activities, biodegradability and antimicrobial properties of n-alkyl glucosides, mannosides and galactosides
journal, December 1990

  • Matsumura, Shuichi; Imai, Kazuyasu; Yoshikawa, Sadao
  • Journal of the American Oil Chemists' Society, Vol. 67, Issue 12
  • DOI: 10.1007/BF02541865

Genome-centric view of carbon processing in thawing permafrost
journal, July 2018


Iron-mediated organic matter decomposition in humid soils can counteract protection
journal, May 2020


Behaviors of glucose decomposition during acid-catalyzed hydrothermal hydrolysis of pretreated Gelidium amansii
journal, July 2012


Untargeted metabolomic profiling of Sphagnum fallax reveals novel antimicrobial metabolites
journal, November 2019

  • Fudyma, Jane D.; Lyon, Jamee; AminiTabrizi, Roya
  • Plant Direct, Vol. 3, Issue 11
  • DOI: 10.1002/pld3.179

Trade-offs in resource allocation among moss species control decomposition in boreal peatlands
journal, November 2008


Glycoside Hydrolases across Environmental Microbial Communities
journal, December 2016


Ab initio prediction of metabolic networks using Fourier transform mass spectrometry data
journal, July 2006


The temperature response of soil microbial efficiency and its feedback to climate
journal, January 2013

  • Frey, Serita D.; Lee, Juhwan; Melillo, Jerry M.
  • Nature Climate Change, Vol. 3, Issue 4
  • DOI: 10.1038/nclimate1796

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

The chemistry and biochemistry of phenolic glycosides
journal, January 1969

  • Hopkinson, Shirley M.
  • Quarterly Reviews, Chemical Society, Vol. 23, Issue 1
  • DOI: 10.1039/qr9692300098

Substrate quality alters the microbial mineralization of added substrate and soil organic carbon
journal, January 2014


Review: Bacteriocins of Lactic Acid Bacteria
journal, August 2001

  • Cintas, L. M.; Casaus, M. P.; Herranz, C.
  • Food Science and Technology International, Vol. 7, Issue 4
  • DOI: 10.1106/R8DE-P6HU-CLXP-5RYT

Graphical Method for Analysis of Ultrahigh-Resolution Broadband Mass Spectra of Natural Organic Matter, the Van Krevelen Diagram
journal, October 2003

  • Kim, Sunghwan; Kramer, Robert W.; Hatcher, Patrick G.
  • Analytical Chemistry, Vol. 75, Issue 20
  • DOI: 10.1021/ac034415p

Sequential extraction protocol for organic matter from soils and sediments using high resolution mass spectrometry
journal, June 2017


Targeted Profiling:  Quantitative Analysis of 1 H NMR Metabolomics Data
journal, July 2006

  • Weljie, Aalim M.; Newton, Jack; Mercier, Pascal
  • Analytical Chemistry, Vol. 78, Issue 13
  • DOI: 10.1021/ac060209g

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


Does dissolved organic matter or solid peat fuel anaerobic respiration in peatlands?
journal, September 2019


FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry
journal, December 2009

  • Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup
  • Analytical Chemistry, Vol. 81, Issue 24
  • DOI: 10.1021/ac9019522

Peatlands in a changing world
journal, June 2011


Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques
journal, July 2013


Biosynthesis of methyl glucoside and its antibacterial activity against Staphylococcus aureus and Escherichia coli
journal, October 2019

  • Kaulpiboon, Jarunee; Rudeekulthamrong, Prakarn
  • Bioactive Carbohydrates and Dietary Fibre, Vol. 20
  • DOI: 10.1016/j.bcdf.2019.100197

The Role of Sphagnum in Peatland Development and Persistence
book,  


MetaNetter 2: A Cytoscape plugin for ab initio network analysis and metabolite feature classification
journal, December 2017


Elemental composition and optical properties reveal changes in dissolved organic matter along a permafrost thaw chronosequence in a subarctic peatland
journal, August 2016

  • Hodgkins, Suzanne B.; Tfaily, Malak M.; Podgorski, David C.
  • Geochimica et Cosmochimica Acta, Vol. 187
  • DOI: 10.1016/j.gca.2016.05.015

Elevated [CO2] changes soil organic matter composition and substrate diversity in an arid ecosystem
journal, November 2018


Using network analysis to discern compositional patterns in ultrahigh-resolution mass spectrometry data of dissolved organic matter: Network analysis and mass spectrometry
journal, September 2016

  • Longnecker, Krista; Kujawinski, Elizabeth B.
  • Rapid Communications in Mass Spectrometry, Vol. 30, Issue 22
  • DOI: 10.1002/rcm.7719

Stabilization and destabilization of soil organic matter: mechanisms and controls
journal, November 1996


Wetlands and the global carbon cycle: what might the simulated past tell us about the future?
journal, November 2011


Impacts of Climate Change on Vegetation Distribution no. 2 - Climate Change Induced Vegetation Shifts in the new World
journal, August 2014


Complete and Partial Photo-oxidation of Dissolved Organic Matter Draining Permafrost Soils
journal, March 2016


Soil physics meets soil biology: Towards better mechanistic prediction of greenhouse gas emissions from soil
journal, April 2012


Microaggregates in soils
journal, August 2017

  • Totsche, Kai Uwe; Amelung, Wulf; Gerzabek, Martin H.
  • Journal of Plant Nutrition and Soil Science, Vol. 181, Issue 1
  • DOI: 10.1002/jpln.201600451

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

Biotic and Abiotic Drivers of Topsoil Organic Carbon Concentration in Drylands Have Similar Effects at Regional and Global Scales
journal, March 2019


Cell-wall polysaccharides play an important role in decay resistance of Sphagnum and actively depressed decomposition in vitro
journal, April 2010


Abiotic drivers and their interactive effect on the flux and carbon isotope (14C and δ13C) composition of peat-respired CO2
journal, December 2011


MetaboliteDetector: Comprehensive Analysis Tool for Targeted and Nontargeted GC/MS Based Metabolome Analysis
journal, May 2009

  • Hiller, Karsten; Hangebrauk, Jasper; Jäger, Christian
  • Analytical Chemistry, Vol. 81, Issue 9
  • DOI: 10.1021/ac802689c

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


Potential shift from a carbon sink to a source in Amazonian peatlands under a changing climate
journal, November 2018

  • Wang, Sirui; Zhuang, Qianlai; Lähteenoja, Outi
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 49
  • DOI: 10.1073/pnas.1801317115

The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008


How Sphagnum bogs down other plants
journal, July 1995


Degradation of natural organic matter: A thermodynamic analysis
journal, April 2011

  • LaRowe, Douglas E.; Van Cappellen, Philippe
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 8
  • DOI: 10.1016/j.gca.2011.01.020