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Title: Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community

Abstract

ABSTRACT Stochasticity emerging from random differences in replication, death, mutation, and dispersal is thought to alter the composition of ecological communities. However, the importance of stochastic effects remains somewhat speculative because stochasticity is not directly measured but is instead inferred from unexplained variations in beta-diversity. Here, we performed a field experiment to more directly disentangle the role of stochastic processes, environmental selection, and dispersal in the composition and functioning of a natural bacterial decomposer community in the field. To increase our ability to detect these effects, we reduced initial biological and environmental heterogeneity using replicate nylon litterbags in the field. We then applied two treatments: ambient/added precipitation and bacterial and fungal dispersal using “open” litterbags (made from 18.0-μm-pore-size mesh) (“open bacterial dispersal”) versus bacterial and fungal dispersal using “closed” litterbags (made from 22.0-μm-pore-size mesh) (“closed bacterial dispersal”). After 5 months, we assayed composition and functioning by the use of three subsamples from each litterbag to disentangle stochastic effects from residual variation. Our results indicate that stochasticity via ecological drift can contribute to beta-diversity in bacterial communities. However, residual variation, which had previously been included in stochasticity estimates, accounted for more than four times as much variability. At the same time,more » stochastic effects on beta-diversity were not attenuated at the functional level, as measured by genetic functional potential and extracellular enzyme activity. Finally, dispersal was found to interact with precipitation availability to influence the degree to which stochasticity contributed to functional variation. Together, our results demonstrate that the ability to quantify stochastic processes is key to understanding microbial diversity and its role in ecosystem functioning. IMPORTANCERandomness can alter the diversity and composition of ecological communities. Such stochasticity may therefore obscure the relationship between the environment and community composition and hinder our ability to predict the relationship between biodiversity and ecosystem functioning. This study investigated the role of stochastic processes, environmental selection, and dispersal in microbial composition and its functioning on an intact field community. To do this, we used a controlled and replicated experiment that was similar to that used to study population genetics in the laboratory. Our study showed that, while the stochastic effects on taxonomic composition are smaller than expected, the degree to which stochasticity contributes to variability in ecosystem processes may be much higher than previously assumed.« less

Authors:
ORCiD logo; ; ;
Publication Date:
Research Org.:
Univ. of California, Irvine, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1507169
Alternate Identifier(s):
OSTI ID: 1626111
Grant/Contract Number:  
SC-SC0016410; PS02-09ER09-25; SC0016410
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 10 Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; beta-diversity; dispersal; ecological drift; ecosystem functioning; stochastic

Citation Formats

Albright, Michaeline B. N., Chase, Alexander B., Martiny, Jennifer B. H., and Taylor, John W. Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community. United States: N. p., 2019. Web. doi:10.1128/mBio.00568-19.
Albright, Michaeline B. N., Chase, Alexander B., Martiny, Jennifer B. H., & Taylor, John W. Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community. United States. doi:10.1128/mBio.00568-19.
Albright, Michaeline B. N., Chase, Alexander B., Martiny, Jennifer B. H., and Taylor, John W. Tue . "Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community". United States. doi:10.1128/mBio.00568-19.
@article{osti_1507169,
title = {Experimental Evidence that Stochasticity Contributes to Bacterial Composition and Functioning in a Decomposer Community},
author = {Albright, Michaeline B. N. and Chase, Alexander B. and Martiny, Jennifer B. H. and Taylor, John W.},
abstractNote = {ABSTRACT Stochasticity emerging from random differences in replication, death, mutation, and dispersal is thought to alter the composition of ecological communities. However, the importance of stochastic effects remains somewhat speculative because stochasticity is not directly measured but is instead inferred from unexplained variations in beta-diversity. Here, we performed a field experiment to more directly disentangle the role of stochastic processes, environmental selection, and dispersal in the composition and functioning of a natural bacterial decomposer community in the field. To increase our ability to detect these effects, we reduced initial biological and environmental heterogeneity using replicate nylon litterbags in the field. We then applied two treatments: ambient/added precipitation and bacterial and fungal dispersal using “open” litterbags (made from 18.0-μm-pore-size mesh) (“open bacterial dispersal”) versus bacterial and fungal dispersal using “closed” litterbags (made from 22.0-μm-pore-size mesh) (“closed bacterial dispersal”). After 5 months, we assayed composition and functioning by the use of three subsamples from each litterbag to disentangle stochastic effects from residual variation. Our results indicate that stochasticity via ecological drift can contribute to beta-diversity in bacterial communities. However, residual variation, which had previously been included in stochasticity estimates, accounted for more than four times as much variability. At the same time, stochastic effects on beta-diversity were not attenuated at the functional level, as measured by genetic functional potential and extracellular enzyme activity. Finally, dispersal was found to interact with precipitation availability to influence the degree to which stochasticity contributed to functional variation. Together, our results demonstrate that the ability to quantify stochastic processes is key to understanding microbial diversity and its role in ecosystem functioning. IMPORTANCERandomness can alter the diversity and composition of ecological communities. Such stochasticity may therefore obscure the relationship between the environment and community composition and hinder our ability to predict the relationship between biodiversity and ecosystem functioning. This study investigated the role of stochastic processes, environmental selection, and dispersal in microbial composition and its functioning on an intact field community. To do this, we used a controlled and replicated experiment that was similar to that used to study population genetics in the laboratory. Our study showed that, while the stochastic effects on taxonomic composition are smaller than expected, the degree to which stochasticity contributes to variability in ecosystem processes may be much higher than previously assumed.},
doi = {10.1128/mBio.00568-19},
journal = {mBio (Online)},
number = 2,
volume = 10,
place = {United States},
year = {2019},
month = {4}
}

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DOI: 10.1128/mBio.00568-19

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Works referenced in this record:

Stochastic Assembly Leads to Alternative Communities with Distinct Functions in a Bioreactor Microbial Community
journal, March 2013


Experimental tests of the bacterial distance–decay relationship
journal, June 2010


Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist: Roadmap for beta diversity
journal, November 2010


Beyond biogeographic patterns: processes shaping the microbial landscape
journal, May 2012

  • Hanson, China A.; Fuhrman, Jed A.; Horner-Devine, M. Claire
  • Nature Reviews Microbiology, Vol. 10, Issue 7
  • DOI: 10.1038/nrmicro2795

The truth about metagenomics: quantifying and counteracting bias in 16S rRNA studies
journal, March 2015


Using null models to disentangle variation in community dissimilarity from variation in α-diversity
journal, February 2011

  • Chase, Jonathan M.; Kraft, Nathan J. B.; Smith, Kevin G.
  • Ecosphere, Vol. 2, Issue 2
  • DOI: 10.1890/ES10-00117.1

Relative roles of niche and neutral processes in structuring a soil microbial community
journal, November 2009

  • Dumbrell, Alex J.; Nelson, Michaela; Helgason, Thorunn
  • The ISME Journal, Vol. 4, Issue 3
  • DOI: 10.1038/ismej.2009.122

Temporal variation of β-diversity and assembly mechanisms in a bacterial metacommunity
journal, December 2011

  • Langenheder, Silke; Berga, Mercè; Östman, Örjan
  • The ISME Journal, Vol. 6, Issue 6
  • DOI: 10.1038/ismej.2011.177

Stochastic Community Assembly: Does It Matter in Microbial Ecology?
journal, October 2017

  • Zhou, Jizhong; Ning, Daliang
  • Microbiology and Molecular Biology Reviews, Vol. 81, Issue 4
  • DOI: 10.1128/MMBR.00002-17

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

Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton
journal, June 2015

  • Apprill, A.; McNally, S.; Parsons, R.
  • Aquatic Microbial Ecology, Vol. 75, Issue 2
  • DOI: 10.3354/ame01753

Conceptual Synthesis in Community Ecology
journal, June 2010

  • Vellend, Mark
  • The Quarterly Review of Biology, Vol. 85, Issue 2
  • DOI: 10.1086/652373

Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession
journal, March 2015

  • Dini-Andreote, Francisco; Stegen, James C.; van Elsas, Jan Dirk
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 11
  • DOI: 10.1073/pnas.1414261112

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

Patterns and Processes of Microbial Community Assembly
journal, September 2013

  • Nemergut, D. R.; Schmidt, S. K.; Fukami, T.
  • Microbiology and Molecular Biology Reviews, Vol. 77, Issue 3
  • DOI: 10.1128/MMBR.00051-12

Disentangling the importance of ecological niches from stochastic processes across scales
journal, August 2011

  • Chase, Jonathan M.; Myers, Jonathan A.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 366, Issue 1576
  • DOI: 10.1098/rstb.2011.0063

Biodiversity of plankton by species oscillations and chaos
journal, November 1999

  • Huisman, Jef; Weissing, Franz J.
  • Nature, Vol. 402, Issue 6760
  • DOI: 10.1038/46540

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


Testing the functional significance of microbial community composition
journal, February 2009

  • Strickland, Michael S.; Lauber, Christian; Fierer, Noah
  • Ecology, Vol. 90, Issue 2
  • DOI: 10.1890/08-0296.1

Drought mediates the importance of stochastic community assembly
journal, October 2007


Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils
journal, September 2013

  • Brown, Shawn P.; Jumpponen, Ari
  • Molecular Ecology, Vol. 23, Issue 2
  • DOI: 10.1111/mec.12487

Distance-Based Tests for Homogeneity of Multivariate Dispersions
journal, October 2005


Stochasticity, succession, and environmental perturbations in a fluidic ecosystem
journal, February 2014

  • Zhou, Jizhong; Deng, Ye; Zhang, Ping
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
  • DOI: 10.1073/pnas.1324044111

Making a microbiome: the many determinants of host-associated microbial community composition
journal, February 2017


Soil pH mediates the balance between stochastic and deterministic assembly of bacteria
journal, March 2018


Decoupling function and taxonomy in the global ocean microbiome
journal, September 2016


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

Stress and stability: applying the Anna Karenina principle to animal microbiomes
journal, August 2017


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


Metagenomic insights into strategies of aerobic and anaerobic carbon and nitrogen transformation in boreal lakes
journal, July 2015

  • Peura, Sari; Sinclair, Lucas; Bertilsson, Stefan
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep12102

Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity
journal, October 2001


The Pfam protein families database: towards a more sustainable future
journal, December 2015

  • Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1344

Fundamental Unpredictability in Multispecies Competition
journal, May 2001

  • Huisman, Jef; Weissing, Franz J.
  • The American Naturalist, Vol. 157, Issue 5
  • DOI: 10.1086/319929

Experimental tests of the roles of adaptation, chance, and history in evolution
journal, January 1995


Repeatability and Contingency in the Evolution of a Key Innovation in Phage Lambda
journal, January 2012


Stochastic assembly produces heterogeneous communities in the Caenorhabditis elegans intestine
journal, March 2017


Dispersal enhances beta diversity in nectar microbes
journal, June 2017

  • Vannette, Rachel L.; Fukami, Tadashi
  • Ecology Letters, Vol. 20, Issue 7
  • DOI: 10.1111/ele.12787

Both species sorting and neutral processes drive assembly of bacterial communities in aquatic microcosms
journal, June 2013

  • Lee, Jack E.; Buckley, Hannah L.; Etienne, Rampal S.
  • FEMS Microbiology Ecology, Vol. 86, Issue 2
  • DOI: 10.1111/1574-6941.12161

Bacterial community assembly based on functional genes rather than species
journal, August 2011

  • Burke, C.; Steinberg, P.; Rusch, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
  • DOI: 10.1073/pnas.1101591108

Changes in assembly processes in soil bacterial communities following a wildfire disturbance
journal, February 2013

  • Ferrenberg, Scott; O'Neill, Sean P.; Knelman, Joseph E.
  • The ISME Journal, Vol. 7, Issue 6
  • DOI: 10.1038/ismej.2013.11

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

Microdiversity of an Abundant Terrestrial Bacterium Encompasses Extensive Variation in Ecologically Relevant Traits
journal, November 2017


PEAR: a fast and accurate Illumina Paired-End reAd mergeR
journal, October 2013


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

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

Microbial legacies alter decomposition in response to simulated global change
journal, October 2016

  • Martiny, Jennifer BH; Martiny, Adam C.; Weihe, Claudia
  • The ISME Journal, Vol. 11, Issue 2
  • DOI: 10.1038/ismej.2016.122

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


Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Profile hidden Markov models
journal, October 1998


Effects of dispersal and selection on stochastic assembly in microbial communities
journal, August 2016

  • Evans, Sarah; Martiny, Jennifer B. H.; Allison, Steven D.
  • The ISME Journal, Vol. 11, Issue 1
  • DOI: 10.1038/ismej.2016.96

Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011


Ecological drift and the distribution of species diversity
journal, May 2017

  • Gilbert, Benjamin; Levine, Jonathan M.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1855
  • DOI: 10.1098/rspb.2017.0507

FragGeneScan-plus for scalable high-throughput short-read open reading frame prediction
conference, August 2015

  • Kim, Dongjae; Hahn, Aria S.; Wu, Shang-Ju
  • 2015 IEEE Conference on Computational Intelligence in Bioinformatics and Computational Biology (CIBCB)
  • DOI: 10.1109/CIBCB.2015.7300341

High taxonomic variability despite stable functional structure across microbial communities
journal, December 2016

  • Louca, Stilianos; Jacques, Saulo M. S.; Pires, Aliny P. F.
  • Nature Ecology & Evolution, Vol. 1, Issue 1
  • DOI: 10.1038/s41559-016-0015

Do assembly history effects attenuate from species to ecosystem properties? A field test with wood-inhabiting fungi: Assembly history effects
journal, December 2011


Climate warming leads to divergent succession of grassland microbial communities
journal, August 2018


Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity
journal, January 2002

  • Hughes, Jennifer B.; Hellmann, Jessica J.; Ricketts, Taylor H.
  • Applied and Environmental Microbiology, Vol. 68, Issue 1
  • DOI: 10.1128/aem.68.1.448