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Title: Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils

Abstract

ABSTRACT As Earth's climate warms, soil carbon pools and the microbial communities that process them may change, altering the way in which carbon is recycled in soil. In this study, we used a combination of metagenomics and bacterial cultivation to evaluate the hypothesis that experimentally raising soil temperatures by 5°C for 5, 8, or 20 years increased the potential for temperate forest soil microbial communities to degrade carbohydrates. Warming decreased the proportion of carbohydrate-degrading genes in the organic horizon derived from eukaryotes and increased the fraction of genes in the mineral soil associated with Actinobacteria in all studies. Genes associated with carbohydrate degradation increased in the organic horizon after 5 years of warming but had decreased in the organic horizon after warming the soil continuously for 20 years. However, a greater proportion of the 295 bacteria from 6 phyla (10 classes, 14 orders, and 34 families) isolated from heated plots in the 20-year experiment were able to depolymerize cellulose and xylan than bacterial isolates from control soils. Together, these findings indicate that the enrichment of bacteria capable of degrading carbohydrates could be important for accelerated carbon cycling in a warmer world. IMPORTANCE The massive carbon stocks currently held in soilsmore » have been built up over millennia, and while numerous lines of evidence indicate that climate change will accelerate the processing of this carbon, it is unclear whether the genetic repertoire of the microbes responsible for this elevated activity will also change. In this study, we showed that bacteria isolated from plots subject to 20 years of 5°C of warming were more likely to depolymerize the plant polymers xylan and cellulose, but that carbohydrate degradation capacity is not uniformly enriched by warming treatment in the metagenomes of soil microbial communities. This study illustrates the utility of combining culture-dependent and culture-independent surveys of microbial communities to improve our understanding of the role changing microbial communities may play in soil carbon cycling under climate change.« less

Authors:
ORCiD logo [1];  [2];  [3];  [2];  [4];  [5];  [2];  [4]; ORCiD logo [6];
  1. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, USA
  2. Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA
  3. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, USA, Department of Biology, University of Massachusetts, Amherst, Massachusetts, USA
  4. Department of Natural Resources and the Environment, University of New Hampshire, Durham, New Hampshire, USA
  5. The Ecosystems Center, Marine Biological Laboratories, Woods Hole, Massachusetts, USA
  6. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, USA, Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA
Publication Date:
Research Org.:
The Marine Biological Laboratory, Woods Hole, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1786374
Alternate Identifier(s):
OSTI ID: 1424727
Grant/Contract Number:  
AC02-05CH11231; SC0010740
Resource Type:
Published Article
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Name: Applied and Environmental Microbiology Journal Volume: 82 Journal Issue: 22; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Pold, Grace, Billings, Andrew F., Blanchard, Jeff L., Burkhardt, Daniel B., Frey, Serita D., Melillo, Jerry M., Schnabel, Julia, van Diepen, Linda T. A., DeAngelis, Kristen M., and Löffler, ed., F. E. Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils. United States: N. p., 2016. Web. doi:10.1128/AEM.02012-16.
Pold, Grace, Billings, Andrew F., Blanchard, Jeff L., Burkhardt, Daniel B., Frey, Serita D., Melillo, Jerry M., Schnabel, Julia, van Diepen, Linda T. A., DeAngelis, Kristen M., & Löffler, ed., F. E. Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils. United States. https://doi.org/10.1128/AEM.02012-16
Pold, Grace, Billings, Andrew F., Blanchard, Jeff L., Burkhardt, Daniel B., Frey, Serita D., Melillo, Jerry M., Schnabel, Julia, van Diepen, Linda T. A., DeAngelis, Kristen M., and Löffler, ed., F. E. Tue . "Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils". United States. https://doi.org/10.1128/AEM.02012-16.
@article{osti_1786374,
title = {Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils},
author = {Pold, Grace and Billings, Andrew F. and Blanchard, Jeff L. and Burkhardt, Daniel B. and Frey, Serita D. and Melillo, Jerry M. and Schnabel, Julia and van Diepen, Linda T. A. and DeAngelis, Kristen M. and Löffler, ed., F. E.},
abstractNote = {ABSTRACT As Earth's climate warms, soil carbon pools and the microbial communities that process them may change, altering the way in which carbon is recycled in soil. In this study, we used a combination of metagenomics and bacterial cultivation to evaluate the hypothesis that experimentally raising soil temperatures by 5°C for 5, 8, or 20 years increased the potential for temperate forest soil microbial communities to degrade carbohydrates. Warming decreased the proportion of carbohydrate-degrading genes in the organic horizon derived from eukaryotes and increased the fraction of genes in the mineral soil associated with Actinobacteria in all studies. Genes associated with carbohydrate degradation increased in the organic horizon after 5 years of warming but had decreased in the organic horizon after warming the soil continuously for 20 years. However, a greater proportion of the 295 bacteria from 6 phyla (10 classes, 14 orders, and 34 families) isolated from heated plots in the 20-year experiment were able to depolymerize cellulose and xylan than bacterial isolates from control soils. Together, these findings indicate that the enrichment of bacteria capable of degrading carbohydrates could be important for accelerated carbon cycling in a warmer world. IMPORTANCE The massive carbon stocks currently held in soils have been built up over millennia, and while numerous lines of evidence indicate that climate change will accelerate the processing of this carbon, it is unclear whether the genetic repertoire of the microbes responsible for this elevated activity will also change. In this study, we showed that bacteria isolated from plots subject to 20 years of 5°C of warming were more likely to depolymerize the plant polymers xylan and cellulose, but that carbohydrate degradation capacity is not uniformly enriched by warming treatment in the metagenomes of soil microbial communities. This study illustrates the utility of combining culture-dependent and culture-independent surveys of microbial communities to improve our understanding of the role changing microbial communities may play in soil carbon cycling under climate change.},
doi = {10.1128/AEM.02012-16},
journal = {Applied and Environmental Microbiology},
number = 22,
volume = 82,
place = {United States},
year = {Tue Nov 15 00:00:00 EST 2016},
month = {Tue Nov 15 00:00:00 EST 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/AEM.02012-16

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Works referenced in this record:

Metatranscriptomic Analysis of Arctic Peat Soil Microbiota
journal, July 2014

  • Tveit, Alexander T.; Urich, Tim; Svenning, Mette M.
  • Applied and Environmental Microbiology, Vol. 80, Issue 18
  • DOI: 10.1128/AEM.01030-14

Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions
journal, March 2012

  • Schneider, Thomas; Keiblinger, Katharina M.; Schmid, Emanuel
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.11

The DOE-JGI Standard Operating Procedure for the Annotations of Microbial Genomes
journal, July 2009

  • Mavromatis, Konstantinos; Ivanova, Natalia N.; Chen, I-Min A.
  • Standards in Genomic Sciences, Vol. 1, Issue 1
  • DOI: 10.4056/sigs.632

Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming
journal, February 2016

  • Xue, Kai; M. Yuan, Mengting; J. Shi, Zhou
  • Nature Climate Change, Vol. 6, Issue 6
  • DOI: 10.1038/nclimate2940

Microbial mediation of carbon-cycle feedbacks to climate warming
journal, December 2011

  • Zhou, Jizhong; Xue, Kai; Xie, Jianping
  • Nature Climate Change, Vol. 2, Issue 2
  • DOI: 10.1038/nclimate1331

Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw
journal, November 2011

  • Mackelprang, Rachel; Waldrop, Mark P.; DeAngelis, Kristen M.
  • Nature, Vol. 480, Issue 7377
  • DOI: 10.1038/nature10576

ggplot2
book, January 2009


Isolation of a Substantial Proportion of Forest Soil Bacterial Communities Detected via Pyrotag Sequencing
journal, January 2013

  • VanInsberghe, David; Hartmann, Martin; Stewart, Gordon R.
  • Applied and Environmental Microbiology, Vol. 79, Issue 6
  • DOI: 10.1128/AEM.03112-12

Bacterial chitin degradation—mechanisms and ecophysiological strategies
journal, January 2013


Assessment of Bias Associated with Incomplete Extraction of Microbial DNA from Soil
journal, June 2009

  • Feinstein, L. M.; Sul, W. J.; Blackwood, C. B.
  • Applied and Environmental Microbiology, Vol. 75, Issue 16
  • DOI: 10.1128/AEM.00120-09

Soil Microbial Community Responses to a Decade of Warming as Revealed by Comparative Metagenomics
journal, December 2013

  • Luo, Chengwei; Rodriguez-R, Luis M.; Johnston, Eric R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 5
  • DOI: 10.1128/AEM.03712-13

Über die Dissociationswärme und den Einfluss der Temperatur auf den Dissociationsgrad der Elektrolyte
journal, January 1889


Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential
journal, January 2011

  • Bandounas, Luaine; Wierckx, Nick JP; de Winde, Johannes H.
  • BMC Biotechnology, Vol. 11, Issue 1
  • DOI: 10.1186/1472-6750-11-94

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

Active and total microbial communities in forest soil are largely different and highly stratified during decomposition
journal, July 2011

  • Baldrian, Petr; Kolařík, Miroslav; Štursová, Martina
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.95

Forest harvesting reduces the soil metagenomic potential for biomass decomposition
journal, April 2015

  • Cardenas, Erick; Kranabetter, J. M.; Hope, Graeme
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.57

Metagenomics of Hydrocarbon Resource Environments Indicates Aerobic Taxa and Genes to be Unexpectedly Common
journal, September 2013

  • An, Dongshan; Caffrey, Sean M.; Soh, Jung
  • Environmental Science & Technology, Vol. 47, Issue 18
  • DOI: 10.1021/es4020184

Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites
journal, March 2014


Selective isolation of bioactive soil actinomycetes belonging to the Streptomyces violaceusniger phenotypic cluster
journal, May 2004


Feature Selection with the Boruta Package
journal, January 2010

  • Kursa, Miron B.; Rudnicki, Witold R.
  • Journal of Statistical Software, Vol. 36, Issue 11
  • DOI: 10.18637/jss.v036.i11

Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation
journal, October 2006


Methods for characterization of Streptomyces species
journal, July 1966

  • Shirling, E. B.; Gottlieb, D.
  • International Journal of Systematic Bacteriology, Vol. 16, Issue 3
  • DOI: 10.1099/00207713-16-3-313

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

Long-term warming restructures Arctic tundra without changing net soil carbon storage
journal, May 2013

  • Sistla, Seeta A.; Moore, John C.; Simpson, Rodney T.
  • Nature, Vol. 497, Issue 7451
  • DOI: 10.1038/nature12129

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Stronger warming effects on microbial abundances in colder regions
journal, December 2015

  • Chen, Ji; Luo, Yiqi; Xia, Jianyang
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep18032

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

Modern Applied Statistics with S
book, August 2002


RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


The Unsolved Challenge to Phylogenetic Correlation Tests for Categorical Characters
journal, September 2014

  • Maddison, Wayne P.; FitzJohn, Richard G.
  • Systematic Biology, Vol. 64, Issue 1
  • DOI: 10.1093/sysbio/syu070

Extracellular DNA extraction is a fast, cheap and reliable alternative for multi-taxa surveys based on soil DNA
journal, May 2016


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Next Generation Sequence Assembly with AMOS
journal, March 2011

  • Treangen, Todd J.; Sommer, Dan D.; Angly, Florent E.
  • Current Protocols in Bioinformatics, Vol. 33, Issue 1
  • DOI: 10.1002/0471250953.bi1108s33

EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences
journal, October 2007

  • Kim, Byung Kwon; Lim, Young-Woon; Kim, Myungjin
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 10
  • DOI: 10.1099/ijs.0.64915-0

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


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

Changes in the seasonal snow cover of alpine regions and its effect on soil processes: A review
journal, March 2007


diArk – the database for eukaryotic genome and transcriptome assemblies in 2014
journal, November 2014

  • Kollmar, Martin; Kollmar, Lotte; Hammesfahr, Björn
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku990

SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

Influence of Plant Polymers on the Distribution and Cultivation of Bacteria in the Phylum Acidobacteria
journal, November 2010

  • Eichorst, Stephanie A.; Kuske, Cheryl R.; Schmidt, Thomas M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 2
  • DOI: 10.1128/AEM.01080-10

A meta-analysis of responses of soil biota to global change
journal, January 2011


Enzymic analysis of microbial pattern and process
journal, January 1994

  • Sinsabaugh, R. S.
  • Biology and Fertility of Soils, Vol. 17, Issue 1
  • DOI: 10.1007/BF00418675

The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study
journal, January 2012


Predicting microbial traits with phylogenies
journal, September 2015


Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter: Seasonal dynamics of a soil microbial community
journal, October 2015

  • Žifčáková, Lucia; Větrovský, Tomáš; Howe, Adina
  • Environmental Microbiology, Vol. 18, Issue 1
  • DOI: 10.1111/1462-2920.13026

Genomic Potential for Polysaccharide Deconstruction in Bacteria
journal, December 2014

  • Berlemont, Renaud; Martiny, Adam C.
  • Applied and Environmental Microbiology, Vol. 81, Issue 4
  • DOI: 10.1128/AEM.03718-14

SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler
journal, December 2012


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

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

The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis
journal, December 2004

  • Cole, J. R.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki038

Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002


Potential of Cometabolic Transformation of Polysaccharides and Lignin in Lignocellulose by Soil Actinobacteria
journal, February 2014


Two decades of warming increases diversity of a potentially lignolytic bacterial community
journal, May 2015


Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level
journal, February 2015


The Pfam protein families database
journal, November 2011

  • Punta, M.; Coggill, P. C.; Eberhardt, R. Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1065

Phylogenetic Logistic Regression for Binary Dependent Variables
journal, November 2009


Soil warming, carbon-nitrogen interactions, and forest carbon budgets
journal, May 2011

  • Melillo, J. M.; Butler, S.; Johnson, J.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 23
  • DOI: 10.1073/pnas.1018189108

Responses of Trace Gas Fluxes and N Availability to Experimentally Elevated Soil Temperatures
journal, August 1994

  • Peterjohn, William T.; Melillo, Jerry M.; Steudler, Paul A.
  • Ecological Applications, Vol. 4, Issue 3
  • DOI: 10.2307/1941962

Thermal adaptation of soil microbial respiration to elevated temperature
journal, December 2008


Community composition and cellulase activity of cellulolytic bacteria from forest soils planted with broad-leaved deciduous and evergreen trees
journal, July 2013

  • Yang, Jiang-Ke; Zhang, Jing-Jing; Yu, Heng-Yu
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 3
  • DOI: 10.1007/s00253-013-5130-4

Microbial biomass, functional capacity, and community structure after 12 years of soil warming
journal, November 2008


A Rapid and Easy Method for the Detection of Microbial Cellulases on Agar Plates Using Gram’s Iodine
journal, September 2008


Profile hidden Markov models
journal, October 1998


Assessing the hydrocarbon degrading potential of indigenous bacteria isolated from crude oil tank bottom sludge and hydrocarbon-contaminated soil of Azzawiya oil refinery, Libya
journal, June 2014

  • Mansur, Abdulatif A.; Adetutu, Eric M.; Kadali, Krishna K.
  • Environmental Science and Pollution Research, Vol. 21, Issue 18
  • DOI: 10.1007/s11356-014-3018-1

Seasonal dynamics of fungal communities in a temperate oak forest soil
journal, September 2013

  • Voříšková, Jana; Brabcová, Vendula; Cajthaml, Tomáš
  • New Phytologist, Vol. 201, Issue 1
  • DOI: 10.1111/nph.12481

Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems
journal, July 2006


Responses of ecosystem carbon cycle to experimental warming: a meta-analysis
journal, March 2013

  • Lu, Meng; Zhou, Xuhui; Yang, Qiang
  • Ecology, Vol. 94, Issue 3
  • DOI: 10.1890/12-0279.1

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Changes in rhizosphere bacterial gene expression following glyphosate treatment
journal, May 2016