Microbial legacies alter decomposition in response to simulated global change

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.

doi:10.1038/ismej.2016.122

Microbial legacies alter decomposition in response to simulated global change

Journal Article · Fri Oct 14 00:00:00 EDT 2016 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2016.122· OSTI ID:1413718

Martiny, Jennifer B. H. ^[1]; Martiny, Adam C. ^[1]; Weihe, Claudia ^[1]; Lu, Ying ^[1]; Berlemont, Renaud ^[2]; Brodie, Eoin L. ^[3]; Goulden, Michael L. ^[1]; Treseder, Kathleen K. ^[1]; Allison, Steven D. ^[1]

Univ. of California, Irvine, CA (United States)
Univ. of California, Irvine, CA (United States); California State Univ. (CalState), Long Beach, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1413718

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 2 Vol. 11; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions Reeder, Jens; Knight, Rob Nature Methods, Vol. 7, Issue 9 https://doi.org/10.1038/nmeth0910-668b	journal	September 2010
Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail Lavorel, S.; Garnier, E. Functional Ecology, Vol. 16, Issue 5 https://doi.org/10.1046/j.1365-2435.2002.00664.x	journal	October 2002
Resilience vs. historical contingency in microbial responses to environmental change Hawkes, Christine V.; Keitt, Timothy H. Ecology Letters, Vol. 18, Issue 7 https://doi.org/10.1111/ele.12451	journal	May 2015
Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems Rousk, Johannes; Smith, Andrew R.; Jones, Davey L. Global Change Biology, Vol. 19, Issue 12 https://doi.org/10.1111/gcb.12338	journal	October 2013
An Evaluation of Techniques for Measuring Vesicular Arbuscular Mycorrhizal Infection in Roots Giovannetti, M.; Mosse, B. New Phytologist, Vol. 84, Issue 3 https://doi.org/10.1111/j.1469-8137.1980.tb04556.x	journal	March 1980
The Application of Ecological Theory Toward an Understanding of the Human Microbiome Costello, E. K.; Stagaman, K.; Dethlefsen, L. Science, Vol. 336, Issue 6086 https://doi.org/10.1126/science.1224203	journal	June 2012
Phylogenetic Distribution of Potential Cellulases in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/aem.03305-12	journal	December 2012
Bacterial Biovolume and Biomass Estimations Bratbak, Gunnar Applied and Environmental Microbiology, Vol. 49, Issue 6 https://doi.org/10.1128/aem.49.6.1488-1493.1985	journal	January 1985
Ecological and Evolutionary Responses to Recent Climate Change Parmesan, Camille Annual Review of Ecology, Evolution, and Systematics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.ecolsys.37.091305.110100	journal	December 2006
Fundamentals of Microbial Community Resistance and Resilience Shade, Ashley; Peter, Hannes; Allison, Steven D. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00417	journal	January 2012
Cellulolytic potential under environmental changes in microbial communities from grassland litter Berlemont, Renaud; Allison, Steven D.; Weihe, Claudia Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00639	journal	November 2014
The Metagenomics RAST Server: A Public Resource for the Automatic Phylogenetic and Functional Analysis of Metagenomes Glass, Elizabeth M.; Meyer, Folker Handbook of Molecular Microbial Ecology I: Metagenomics and Complementary Approaches https://doi.org/10.1002/9781118010518.ch37	book	January 2011
Response of Microbial Community Composition and Function to Soil Climate Change Waldrop, M. P.; Firestone, M. K. Microbial Ecology, Vol. 52, Issue 4 https://doi.org/10.1007/s00248-006-9103-3	journal	October 2006
Integrating microbial ecology into ecosystem models: challenges and priorities Treseder, Kathleen K.; Balser, Teri C.; Bradford, Mark A. Biogeochemistry, Vol. 109, Issue 1-3 https://doi.org/10.1007/s10533-011-9636-5	journal	September 2011
Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Evans, Sarah E.; Wallenstein, Matthew D. Biogeochemistry, Vol. 109, Issue 1-3 https://doi.org/10.1007/s10533-011-9638-3	journal	September 2011
Integrating ecology into biotechnology McMahon, Katherine D.; Martin, Hector Garcia; Hugenholtz, Philip Current Opinion in Biotechnology, Vol. 18, Issue 3 https://doi.org/10.1016/j.copbio.2007.04.007	journal	June 2007
Ecological effects of experimental drought and prescribed fire in a southern California coastal grassland Potts, D. L.; Suding, K. N.; Winston, G. C. Journal of Arid Environments, Vol. 81 https://doi.org/10.1016/j.jaridenv.2012.01.007	journal	June 2012
Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment Lawrence, Corey R.; Neff, Jason C.; Schimel, Joshua P. Soil Biology and Biochemistry, Vol. 41, Issue 9 https://doi.org/10.1016/j.soilbio.2009.06.016	journal	September 2009
Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland Alster, Charlotte J.; German, Donovan P.; Lu, Ying Soil Biology and Biochemistry, Vol. 64 https://doi.org/10.1016/j.soilbio.2013.03.034	journal	September 2013
Legacy effects of elevated ozone on soil biota and plant growth Li, Qi; Yang, Yue; Bao, Xuelian Soil Biology and Biochemistry, Vol. 91 https://doi.org/10.1016/j.soilbio.2015.08.029	journal	December 2015
Generalized Eta and Omega Squared Statistics: Measures of Effect Size for Some Common Research Designs. Olejnik, Stephen; Algina, James Psychological Methods, Vol. 8, Issue 4 https://doi.org/10.1037/1082-989X.8.4.434	journal	January 2003
Temporal variation overshadows the response of leaf litter microbial communities to simulated global change Matulich, Kristin L.; Weihe, Claudia; Allison, Steven D. The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.58	journal	May 2015
Microbial response to simulated global change is phylogenetically conserved and linked with functional potential Amend, Anthony S.; Martiny, Adam C.; Allison, Steven D. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.96	journal	June 2015
Diversity, stability and resilience of the human gut microbiota Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I. Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11550	journal	September 2012
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Microbial community structure and global trace gases Schimel, Joshua P.; Gulledge, Jay. Global Change Biology, Vol. 4, Issue 7 https://doi.org/10.1046/j.1365-2486.1998.00195.x	journal	October 1998
A new method for non-parametric multivariate analysis of variance Anderson, Marti J. Austral Ecology, Vol. 26, Issue 1 https://doi.org/10.1046/j.1442-9993.2001.01070.x	journal	February 2001
Resistance, resilience, and redundancy in microbial communities Allison, S. D.; Martiny, J. B. H. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0801925105	journal	August 2008
Lagging adaptation to warming climate in Arabidopsis thaliana Wilczek, A. M.; Cooper, M. D.; Korves, T. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1406314111	journal	May 2014
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Ribosomal Database Project: data and tools for high throughput rRNA analysis Cole, James R.; Wang, Qiong; Fish, Jordan A. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1244	journal	November 2013
Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates Adair, E. Carol; Parton, William J.; Del Grosso, Steven J. Global Change Biology https://doi.org/10.1111/j.1365-2486.2008.01674.x	journal	August 2008
Testing the functional significance of microbial composition in natural communities: Functional significance of microbial composition Reed, Heather E.; Martiny, Jennifer B. H. FEMS Microbiology Ecology, Vol. 62, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00386.x	journal	November 2007
Microbiomes in light of traits: A phylogenetic perspective Martiny, J. B. H.; Jones, S. E.; Lennon, J. T. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aac9323	journal	November 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
Phylogenetic Distribution of Potential Cellulases in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/AEM.03305-12	journal	December 2012
Genomic Potential for Polysaccharide Deconstruction in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 81, Issue 4 https://doi.org/10.1128/AEM.03718-14	journal	December 2014
Bacterial Biovolume and Biomass Estimations Bratbak, Gunnar Applied and Environmental Microbiology, Vol. 49, Issue 6 https://doi.org/10.1128/AEM.49.6.1488-1493.1985	journal	January 1985
Decomposition in Terrestrial Ecosystems Swift, M. J.; Heal, O. W.; Anderson, J. M. https://doi.org/10.1525/9780520407114	book	December 1979
Microbial abundance and composition influence litter decomposition response to environmental change Allison, Steven D.; Lu, Ying; Weihe, Claudia Ecology, Vol. 94, Issue 3 https://doi.org/10.1890/12-1243.1	journal	March 2013
Altered water and nitrogen input shifts succession in a southern California coastal sage community Kimball, Sarah; Goulden, Michael L.; Suding, Katharine N. Ecological Applications, Vol. 24, Issue 6 https://doi.org/10.1890/13-1313.1	journal	September 2014
Altered water and nitrogen input shifts succession in a southern California coastal sage community Kimball, Sarah; Goulden, Michael L.; Suding, Katharine N. Figshare https://doi.org/10.6084/m9.figshare.c.3296363	collection	January 2016
Microbial abundance and composition influence litter decomposition response to environmental change D. Allison, Steven; Lu, Ying; Weihe, Claudia Wiley https://doi.org/10.6084/m9.figshare.c.3305403	collection	January 2016

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Drought increases the frequencies of fungal functional genes related to carbon and nitrogen acquisition Treseder, Kathleen K.; Berlemont, Renaud; Allison, Steven D. PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0206441	journal	November 2018
Drought Stress and Root-Associated Bacterial Communities Naylor, Dan; Coleman-Derr, Devin Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02223	journal	January 2018
Necrobiome Framework for Bridging Decomposition Ecology of Autotrophically and Heterotrophically Derived Organic Matter Benbow, Mark Eric; Barton, Philip S.; Ulyshen, Michael D. The Bulletin of the Ecological Society of America, Vol. 100, Issue 1 https://doi.org/10.1002/bes2.1454	journal	January 2019
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Genomic adaptation of marine phytoplankton populations regulates phosphate uptake Martiny, Adam C.; Ustick, Lucas; A. Garcia, Catherine Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11252	journal	January 2020
Historical Drought Affects Microbial Population Dynamics and Activity During Soil Drying and Re-Wet Veach, Allison M.; Zeglin, Lydia H. Microbial Ecology, Vol. 79, Issue 3 https://doi.org/10.1007/s00248-019-01432-5	journal	September 2019
Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard) Anthony, M. A.; Stinson, K. A.; Trautwig, A. N. Biological Invasions, Vol. 21, Issue 10 https://doi.org/10.1007/s10530-019-02031-8	journal	June 2019
Flooding and prolonged drought have differential legacy impacts on soil nitrogen cycling, microbial communities and plant productivity Nguyen, Linh T. T.; Osanai, Yui; Anderson, Ian C. Plant and Soil, Vol. 431, Issue 1-2 https://doi.org/10.1007/s11104-018-3774-7	journal	August 2018
Dispersal alters bacterial diversity and composition in a natural community Albright, Michaeline B. N.; Martiny, Jennifer B. H. The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.161	journal	October 2017
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Drought and its legacy modulate the post‐fire recovery of soil functionality and microbial community structure in a Mediterranean shrubland Hinojosa, María Belén; Laudicina, Vito Armando; Parra, Antonio Global Change Biology, Vol. 25, Issue 4 https://doi.org/10.1111/gcb.14575	journal	February 2019
Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales Glassman, Sydney I.; Wang, Ian J.; Bruns, Thomas D. Molecular Ecology, Vol. 26, Issue 24 https://doi.org/10.1111/mec.14414	journal	November 2017
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