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Title: Effects of warming on bacterial growth rates in a peat soil under ambient and elevated CO2

Abstract

Boreal peatlands are important global carbon reservoirs that are particularly vulnerable to predicted climate changes such as increasing CO2 and temperature. Since microbial activities regulate the balance of carbon sequestered into soil organic matter or remineralized to CO2, characterizing their response to these environmental factors is critical to predicting how peatland ecosystems will affect climate-carbon cycle feedbacks. Here we examined in-situ taxon-specific variation in microbial growth under long-term elevated CO2 and across a gradient of warming treatments in a northern Minnesota peat bog using quantitative stable isotope probing with 18O-water. Across temperatures, bacterial taxa were grouped according to the excess atom fraction 18O (EAF) of their genomes, a proxy for DNA replication and hence, growth. Taxon-specific growth across CO2 and temperature treatments clustered into relatively few response patterns. While a large portion of taxa showed little to no growth under ambient CO2, many of the same taxa grew rapidly under elevated CO2. We found support for phylogenetic conservation of response patterns among Acidobacteria and Proteobacteria, the two most abundant phyla in our data. Our results suggest certain taxa may be primed for new climate conditions and have a greater influence on carbon cycling with implications for future climate mitigation strategies.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Northern Arizona Univ., Flagstaff, AZ (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Iowa State Univ., Ames, IA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1909596
Alternate Identifier(s):
OSTI ID: 1960958
Report Number(s):
PNNL-SA-166721
Journal ID: ISSN 0038-0717
Grant/Contract Number:  
AC05-76RL01830; AC05-00OR22725; FWP 68907; FWP 74475; SC0020172; SC0016207; AC05- 00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Soil Biology and Biochemistry
Additional Journal Information:
Journal Volume: 178; Journal ID: ISSN 0038-0717
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 16S amplicon sequencing, Carbon Dioxide (CO2), peatlands, warming, microbial ecology, microbial growth, 18O labeling

Citation Formats

Bell, Sheryl L., Zimmerman, Amy E., Stone, Bram W. G, Chang, Christine H., Blumer, Madison R., Renslow, Ryan S., Propster, Jeffrey R., Hayer, Michaela, Schwartz, Egbert, Hungate, Bruce A., and Hofmockel, Kirsten S. Effects of warming on bacterial growth rates in a peat soil under ambient and elevated CO2. United States: N. p., 2022. Web. doi:10.1016/j.soilbio.2022.108933.
Bell, Sheryl L., Zimmerman, Amy E., Stone, Bram W. G, Chang, Christine H., Blumer, Madison R., Renslow, Ryan S., Propster, Jeffrey R., Hayer, Michaela, Schwartz, Egbert, Hungate, Bruce A., & Hofmockel, Kirsten S. Effects of warming on bacterial growth rates in a peat soil under ambient and elevated CO2. United States. https://doi.org/10.1016/j.soilbio.2022.108933
Bell, Sheryl L., Zimmerman, Amy E., Stone, Bram W. G, Chang, Christine H., Blumer, Madison R., Renslow, Ryan S., Propster, Jeffrey R., Hayer, Michaela, Schwartz, Egbert, Hungate, Bruce A., and Hofmockel, Kirsten S. Sat . "Effects of warming on bacterial growth rates in a peat soil under ambient and elevated CO2". United States. https://doi.org/10.1016/j.soilbio.2022.108933. https://www.osti.gov/servlets/purl/1909596.
@article{osti_1909596,
title = {Effects of warming on bacterial growth rates in a peat soil under ambient and elevated CO2},
author = {Bell, Sheryl L. and Zimmerman, Amy E. and Stone, Bram W. G and Chang, Christine H. and Blumer, Madison R. and Renslow, Ryan S. and Propster, Jeffrey R. and Hayer, Michaela and Schwartz, Egbert and Hungate, Bruce A. and Hofmockel, Kirsten S.},
abstractNote = {Boreal peatlands are important global carbon reservoirs that are particularly vulnerable to predicted climate changes such as increasing CO2 and temperature. Since microbial activities regulate the balance of carbon sequestered into soil organic matter or remineralized to CO2, characterizing their response to these environmental factors is critical to predicting how peatland ecosystems will affect climate-carbon cycle feedbacks. Here we examined in-situ taxon-specific variation in microbial growth under long-term elevated CO2 and across a gradient of warming treatments in a northern Minnesota peat bog using quantitative stable isotope probing with 18O-water. Across temperatures, bacterial taxa were grouped according to the excess atom fraction 18O (EAF) of their genomes, a proxy for DNA replication and hence, growth. Taxon-specific growth across CO2 and temperature treatments clustered into relatively few response patterns. While a large portion of taxa showed little to no growth under ambient CO2, many of the same taxa grew rapidly under elevated CO2. We found support for phylogenetic conservation of response patterns among Acidobacteria and Proteobacteria, the two most abundant phyla in our data. Our results suggest certain taxa may be primed for new climate conditions and have a greater influence on carbon cycling with implications for future climate mitigation strategies.},
doi = {10.1016/j.soilbio.2022.108933},
journal = {Soil Biology and Biochemistry},
number = ,
volume = 178,
place = {United States},
year = {Sat Dec 24 00:00:00 EST 2022},
month = {Sat Dec 24 00:00:00 EST 2022}
}

Works referenced in this record:

The general stochastic model of nucleotide substitution
journal, February 1990


Decomposition of peatland DOC affected by root exudates is driven by specific r and K strategic bacterial taxa
journal, September 2021


Experimental warming effects on the microbial community of a temperate mountain forest soil
journal, July 2011


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

Temperature sensitivity of SOM decomposition is linked with a K‐selected microbial community
journal, March 2021

  • Li, Hui; Yang, Shan; Semenov, Mikhail V.
  • Global Change Biology, Vol. 27, Issue 12
  • DOI: 10.1111/gcb.15593

Elevated Carbon Dioxide Alters the Structure of Soil Microbial Communities
journal, February 2012

  • Deng, Ye; He, Zhili; Xu, Meiying
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.06924-11

Soil microorganisms respond to five years of climate change manipulations and elevated atmospheric CO2 in a temperate heath ecosystem
journal, August 2013

  • Haugwitz, Merian Skouw; Bergmark, Lasse; Priemé, Anders
  • Plant and Soil, Vol. 374, Issue 1-2
  • DOI: 10.1007/s11104-013-1855-1

Short-term responses of microbial community and functioning to experimental CO2 enrichment and warming in a Chinese paddy field
journal, October 2014


Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change
journal, September 2019

  • Malik, Ashish A.; Martiny, Jennifer B. H.; Brodie, Eoin L.
  • The ISME Journal, Vol. 14, Issue 1
  • DOI: 10.1038/s41396-019-0510-0

Bacterial Tradeoffs in Growth Rate and Extracellular Enzymes
journal, December 2019


Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide: Soil bacterial response in six ecosystems
journal, January 2012


Life and death in the soil microbiome: how ecological processes influence biogeochemistry
journal, February 2022

  • Sokol, Noah W.; Slessarev, Eric; Marschmann, Gianna L.
  • Nature Reviews Microbiology, Vol. 20, Issue 7
  • DOI: 10.1038/s41579-022-00695-z

Rapid expansion of northern peatlands and doubled estimate of carbon storage
journal, October 2019


Nitrogen and phosphorus cycling in an ombrotrophic peatland: a benchmark for assessing change
journal, July 2021


Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

Interactions between Elevated CO 2 and Warming Could Amplify DOC Exports from Peatland Catchments
journal, May 2007

  • Fenner, Nathalie; Freeman, Christopher; Lock, Maurice A.
  • Environmental Science & Technology, Vol. 41, Issue 9
  • DOI: 10.1021/es061765v

Elevated CO 2 shifts soil microbial communities from K ‐ to r ‐strategists
journal, March 2021

  • Sun, Yuan; Wang, Cuiting; Yang, Jinyan
  • Global Ecology and Biogeography, Vol. 30, Issue 5
  • DOI: 10.1111/geb.13281

Elevated atmospheric CO 2 increases microbial growth rates in soil: results of three CO 2 enrichment experiments
journal, February 2010


Massive peatland carbon banks vulnerable to rising temperatures
journal, May 2020


Quantitative Microbial Ecology through Stable Isotope Probing
journal, August 2015

  • Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert
  • Applied and Environmental Microbiology, Vol. 81, Issue 21
  • DOI: 10.1128/AEM.02280-15

Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter
journal, April 2017

  • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.43

Effects of climate warming on carbon fluxes in grasslands— A global meta‐analysis
journal, February 2019

  • Wang, Na; Quesada, Benjamin; Xia, Longlong
  • Global Change Biology, Vol. 25, Issue 5
  • DOI: 10.1111/gcb.14603

Warming-induced greenhouse gas fluxes from global croplands modified by agricultural practices: A meta-analysis
journal, May 2022


Microbial communities and their responses to simulated global change fluctuate greatly over multiple years
journal, April 2012


SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012


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

Elevated CO2 and Warming Altered Grassland Microbial Communities in Soil Top-Layers
journal, August 2018


Efficient comparative phylogenetics on large trees
journal, October 2017


Accelerated microbial turnover but constant growth efficiency with warming in soil
journal, September 2014

  • Hagerty, Shannon B.; van Groenigen, Kees Jan; Allison, Steven D.
  • Nature Climate Change, Vol. 4, Issue 10
  • DOI: 10.1038/nclimate2361

The temperature sensitivity of soil: microbial biodiversity, growth, and carbon mineralization
journal, March 2021


Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
journal, July 2019


Quantitative stable isotope probing with H 2 18 O to measure taxon‐specific microbial growth
journal, September 2020

  • Purcell, Alicia M.; Dijkstra, Paul; Finley, Brianna
  • Soil Science Society of America Journal, Vol. 84, Issue 5
  • DOI: 10.1002/saj2.20159

phangorn: phylogenetic analysis in R
journal, December 2010


Experimental warming alters the community composition, diversity, and N 2 fixation activity of peat moss ( Sphagnum fallax ) microbiomes
journal, May 2019

  • Carrell, Alyssa A.; Kolton, Max; Glass, Jennifer B.
  • Global Change Biology, Vol. 25, Issue 9
  • DOI: 10.1111/gcb.14715

Interactions between plant growth and soil nutrient cycling under elevated CO 2 : a meta-analysis
journal, November 2006


Minimizing artifacts and biases in chamber-based measurements of soil respiration
journal, December 2002


Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015

  • DeAngelis, Kristen M.; Pold, Grace; TopçuoÄŸlu, Begüm D.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00104

Microbial control over carbon cycling in soil
journal, January 2012


Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2
journal, November 2014

  • Sulman, Benjamin N.; Phillips, Richard P.; Oishi, A. Christopher
  • Nature Climate Change, Vol. 4, Issue 12
  • DOI: 10.1038/nclimate2436

Thermodynamic Control of the Carbon Budget of a Peatland
journal, June 2018

  • Worrall, Fred; Moody, Catherine S.; Clay, Gareth D.
  • Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 6
  • DOI: 10.1029/2017JG003996

Phylogenetic conservation of soil bacterial responses to simulated global changes
journal, March 2020

  • Isobe, Kazuo; Bouskill, Nicholas J.; Brodie, Eoin L.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
  • DOI: 10.1098/rstb.2019.0242

Peatland warming strongly increases fine-root growth
journal, July 2020

  • Malhotra, Avni; Brice, Deanne J.; Childs, Joanne
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 30
  • DOI: 10.1073/pnas.2003361117

Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide
journal, January 2004


Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog
journal, October 2019

  • Norby, Richard J.; Childs, Joanne; Hanson, Paul J.
  • Ecology and Evolution, Vol. 9, Issue 22
  • DOI: 10.1002/ece3.5722

Rapid Net Carbon Loss From a Whole‐Ecosystem Warmed Peatland
journal, July 2020

  • Hanson, Paul J.; Griffiths, Natalie A.; Iversen, Colleen M.
  • AGU Advances, Vol. 1, Issue 3
  • DOI: 10.1029/2020AV000163

Recent Understanding of Soil Acidobacteria and Their Ecological Significance: A Critical Review
journal, October 2020


Response of soil greenhouse gas fluxes to warming: A global meta‐analysis of field studies
journal, August 2022


Expert assessment of future vulnerability of the global peatland carbon sink
journal, December 2020


Response of soil respiration and its components to experimental warming and water addition in a temperate Sitka spruce forest ecosystem
journal, October 2018


Elevated CO2 Effects on Peatland Plant Community Carbon Dynamics and DOC Production
journal, May 2007


Soil microbiomes and climate change
journal, October 2019


Decreased growth of wild soil microbes after 15 years of transplant‐induced warming in a montane meadow
journal, October 2021

  • Purcell, Alicia M.; Hayer, Michaela; Koch, Benjamin J.
  • Global Change Biology, Vol. 28, Issue 1
  • DOI: 10.1111/gcb.15911

Review and synthesis of the effects of elevated atmospheric CO2 on soil processes: No changes in pools, but increased fluxes and accelerated cycles
journal, January 2019


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