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

Title: Microbial legacies alter decomposition in response to simulated global change

Abstract

Terrestrial ecosystem models assume that microbial communities respond instantaneously, or are immediately resilient, to environmental change. Here we tested this assumption by quantifying the resilience of a leaf litter community to changes in precipitation or nitrogen availability. By manipulating composition within a global change experiment, we decoupled the legacies of abiotic parameters versus that of the microbial community itself. After one rainy season, more variation in fungal composition could be explained by the original microbial inoculum than the litterbag environment (18% versus 5.5% of total variation). This compositional legacy persisted for 3 years, when 6% of the variability in fungal composition was still explained by the microbial origin. In contrast, bacterial composition was generally more resilient than fungal composition. Microbial functioning (measured as decomposition rate) was not immediately resilient to the global change manipulations; decomposition depended on both the contemporary environment and rainfall the year prior. Finally, using metagenomic sequencing, we showed that changes in precipitation, but not nitrogen availability, altered the potential for bacterial carbohydrate degradation, suggesting why the functional consequences of the two experiments may have differed. Predictions of how terrestrial ecosystem processes respond to environmental change may thus be improved by considering the legacies of microbial communities.

Authors:
 [1];  [1];  [1];  [1];  [2];  [3];  [1];  [1];  [1]
  1. Univ. of California, Irvine, CA (United States)
  2. Univ. of California, Irvine, CA (United States); California State Univ. (CalState), Long Beach, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1413718
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 11; Journal Issue: 2; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Martiny, Jennifer B. H., Martiny, Adam C., Weihe, Claudia, Lu, Ying, Berlemont, Renaud, Brodie, Eoin L., Goulden, Michael L., Treseder, Kathleen K., and Allison, Steven D. Microbial legacies alter decomposition in response to simulated global change. United States: N. p., 2016. Web. doi:10.1038/ismej.2016.122.
Martiny, Jennifer B. H., Martiny, Adam C., Weihe, Claudia, Lu, Ying, Berlemont, Renaud, Brodie, Eoin L., Goulden, Michael L., Treseder, Kathleen K., & Allison, Steven D. Microbial legacies alter decomposition in response to simulated global change. United States. https://doi.org/10.1038/ismej.2016.122
Martiny, Jennifer B. H., Martiny, Adam C., Weihe, Claudia, Lu, Ying, Berlemont, Renaud, Brodie, Eoin L., Goulden, Michael L., Treseder, Kathleen K., and Allison, Steven D. Fri . "Microbial legacies alter decomposition in response to simulated global change". United States. https://doi.org/10.1038/ismej.2016.122. https://www.osti.gov/servlets/purl/1413718.
@article{osti_1413718,
title = {Microbial legacies alter decomposition in response to simulated global change},
author = {Martiny, Jennifer B. H. and Martiny, Adam C. and Weihe, Claudia and Lu, Ying and Berlemont, Renaud and Brodie, Eoin L. and Goulden, Michael L. and Treseder, Kathleen K. and Allison, Steven D.},
abstractNote = {Terrestrial ecosystem models assume that microbial communities respond instantaneously, or are immediately resilient, to environmental change. Here we tested this assumption by quantifying the resilience of a leaf litter community to changes in precipitation or nitrogen availability. By manipulating composition within a global change experiment, we decoupled the legacies of abiotic parameters versus that of the microbial community itself. After one rainy season, more variation in fungal composition could be explained by the original microbial inoculum than the litterbag environment (18% versus 5.5% of total variation). This compositional legacy persisted for 3 years, when 6% of the variability in fungal composition was still explained by the microbial origin. In contrast, bacterial composition was generally more resilient than fungal composition. Microbial functioning (measured as decomposition rate) was not immediately resilient to the global change manipulations; decomposition depended on both the contemporary environment and rainfall the year prior. Finally, using metagenomic sequencing, we showed that changes in precipitation, but not nitrogen availability, altered the potential for bacterial carbohydrate degradation, suggesting why the functional consequences of the two experiments may have differed. Predictions of how terrestrial ecosystem processes respond to environmental change may thus be improved by considering the legacies of microbial communities.},
doi = {10.1038/ismej.2016.122},
journal = {The ISME Journal},
number = 2,
volume = 11,
place = {United States},
year = {Fri Oct 14 00:00:00 EDT 2016},
month = {Fri Oct 14 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 86 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Ecological and Evolutionary Responses to Recent Climate Change
journal, December 2006


Ecological and Evolutionary Responses to Recent Climate Change
journal, December 2006


A new method for non-parametric multivariate analysis of variance
journal, February 2001


Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Cellulolytic potential under environmental changes in microbial communities from grassland litter
journal, November 2014


Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Phylogenetic Distribution of Potential Cellulases in Bacteria
journal, December 2012

  • Berlemont, Renaud; Martiny, Adam C.
  • Applied and Environmental Microbiology, Vol. 79, Issue 5
  • DOI: 10.1128/AEM.03305-12

Legacy effects of elevated ozone on soil biota and plant growth
journal, December 2015


An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots
journal, March 1980


Microbial response to simulated global change is phylogenetically conserved and linked with functional potential
journal, June 2015

  • Amend, Anthony S.; Martiny, Adam C.; Allison, Steven D.
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.96

Integrating ecology into biotechnology
journal, June 2007

  • McMahon, Katherine D.; Martin, Hector Garcia; Hugenholtz, Philip
  • Current Opinion in Biotechnology, Vol. 18, Issue 3
  • DOI: 10.1016/j.copbio.2007.04.007

The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015


Cellulolytic potential under environmental changes in microbial communities from grassland litter
journal, November 2014


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

Temporal variation overshadows the response of leaf litter microbial communities to simulated global change
journal, May 2015

  • Matulich, Kristin L.; Weihe, Claudia; Allison, Steven D.
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.58

Resistance, resilience, and redundancy in microbial communities
journal, August 2008

  • Allison, S. D.; Martiny, J. B. H.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
  • DOI: 10.1073/pnas.0801925105

Bacterial Biovolume and Biomass Estimations
journal, January 1985


Diversity, stability and resilience of the human gut microbiota
journal, September 2012

  • Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I.
  • Nature, Vol. 489, Issue 7415
  • DOI: 10.1038/nature11550

Microbial abundance and composition influence litter decomposition response to environmental change
journal, March 2013

  • Allison, Steven D.; Lu, Ying; Weihe, Claudia
  • Ecology, Vol. 94, Issue 3
  • DOI: 10.1890/12-1243.1

Ribosomal Database Project: data and tools for high throughput rRNA analysis
journal, November 2013

  • Cole, James R.; Wang, Qiong; Fish, Jordan A.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1244

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


An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots
journal, March 1980


Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems
journal, October 2013

  • Rousk, Johannes; Smith, Andrew R.; Jones, Davey L.
  • Global Change Biology, Vol. 19, Issue 12
  • DOI: 10.1111/gcb.12338

Resilience vs. historical contingency in microbial responses to environmental change
journal, May 2015

  • Hawkes, Christine V.; Keitt, Timothy H.
  • Ecology Letters, Vol. 18, Issue 7
  • DOI: 10.1111/ele.12451

Microbial community structure and global trace gases
journal, October 1998


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

Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions
journal, September 2010


Ecological effects of experimental drought and prescribed fire in a southern California coastal grassland
journal, June 2012


Response of Microbial Community Composition and Function to Soil Climate Change
journal, October 2006


Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions
journal, September 2010


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Generalized Eta and Omega Squared Statistics: Measures of Effect Size for Some Common Research Designs.
journal, January 2003


Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems
journal, October 2013

  • Rousk, Johannes; Smith, Andrew R.; Jones, Davey L.
  • Global Change Biology, Vol. 19, Issue 12
  • DOI: 10.1111/gcb.12338

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

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

Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment
journal, September 2009


Altered water and nitrogen input shifts succession in a southern California coastal sage community
journal, September 2014

  • Kimball, Sarah; Goulden, Michael L.; Suding, Katharine N.
  • Ecological Applications, Vol. 24, Issue 6
  • DOI: 10.1890/13-1313.1

Lagging adaptation to warming climate in Arabidopsis thaliana
journal, May 2014

  • Wilczek, A. M.; Cooper, M. D.; Korves, T. M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
  • DOI: 10.1073/pnas.1406314111

Resilience vs. historical contingency in microbial responses to environmental change
journal, May 2015

  • Hawkes, Christine V.; Keitt, Timothy H.
  • Ecology Letters, Vol. 18, Issue 7
  • DOI: 10.1111/ele.12451

The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland
journal, September 2013


Testing the functional significance of microbial composition in natural communities: Functional significance of microbial composition
journal, November 2007


Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?
journal, September 2011


Integrating microbial ecology into ecosystem models: challenges and priorities
journal, September 2011

  • Treseder, Kathleen K.; Balser, Teri C.; Bradford, Mark A.
  • Biogeochemistry, Vol. 109, Issue 1-3
  • DOI: 10.1007/s10533-011-9636-5

Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates
journal, August 2008


Works referencing / citing this record:

Dispersal alters bacterial diversity and composition in a natural community
journal, October 2017

  • Albright, Michaeline B. N.; Martiny, Jennifer B. H.
  • The ISME Journal, Vol. 12, Issue 1
  • DOI: 10.1038/ismej.2017.161

Drought Stress and Root-Associated Bacterial Communities
journal, January 2018


Historical Drought Affects Microbial Population Dynamics and Activity During Soil Drying and Re-Wet
journal, September 2019


Genomic adaptation of marine phytoplankton populations regulates phosphate uptake
journal, January 2020

  • Martiny, Adam C.; Ustick, Lucas; A. Garcia, Catherine
  • Limnology and Oceanography, Vol. 65, Issue S1
  • DOI: 10.1002/lno.11252

Decomposition responses to climate depend on microbial community composition
journal, November 2018

  • Glassman, Sydney I.; Weihe, Claudia; Li, Junhui
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 47
  • DOI: 10.1073/pnas.1811269115

Microbiome functioning depends on individual and interactive effects of the environment and community structure
journal, July 2018


Flooding and prolonged drought have differential legacy impacts on soil nitrogen cycling, microbial communities and plant productivity
journal, August 2018


Necrobiome framework for bridging decomposition ecology of autotrophically and heterotrophically derived organic matter
journal, September 2018

  • Benbow, M. Eric; Barton, Philip S.; Ulyshen, Michael D.
  • Ecological Monographs, Vol. 89, Issue 1
  • DOI: 10.1002/ecm.1331

Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition
journal, November 2018


Stochastic microbial community assembly decreases biogeochemical function
posted_content, October 2017


Drought and its legacy modulate the post‐fire recovery of soil functionality and microbial community structure in a Mediterranean shrubland
journal, February 2019

  • Hinojosa, María Belén; Laudicina, Vito Armando; Parra, Antonio
  • Global Change Biology, Vol. 25, Issue 4
  • DOI: 10.1111/gcb.14575

Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard)
journal, June 2019


Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales
journal, November 2017

  • Glassman, Sydney I.; Wang, Ian J.; Bruns, Thomas D.
  • Molecular Ecology, Vol. 26, Issue 24
  • DOI: 10.1111/mec.14414

Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition
journal, November 2018


Necrobiome Framework for Bridging Decomposition Ecology of Autotrophically and Heterotrophically Derived Organic Matter
journal, January 2019

  • Benbow, Mark Eric; Barton, Philip S.; Ulyshen, Michael D.
  • The Bulletin of the Ecological Society of America, Vol. 100, Issue 1
  • DOI: 10.1002/bes2.1454

Drought Stress and Root-Associated Bacterial Communities
journal, January 2018


Microbiome functioning depends on individual and interactive effects of the environment and community structure.
text, January 2019

  • Orland, Chloe; Emilson, Erik JS; Basiliko, Nathan
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.26946