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Title: Dispersal-Based Microbial Community Assembly Decreases Biogeochemical Function

Abstract

Ecological mechanisms influence relationships among microbial communities, which in turn impact biogeochemistry. In particular, microbial communities are assembled by deterministic (e.g., selection) and stochastic (e.g., dispersal) processes, and the relative balance of these two process types is hypothesized to alter the influence of microbial communities over biogeochemical function. We used an ecological simulation model to evaluate this hypothesis, defining biogeochemical function generically to represent any biogeochemical reaction of interest. We assembled receiving communities under different levels of dispersal from a source community that was assembled purely by selection. The dispersal scenarios ranged from no dispersal (i.e., selection-only) to dispersal rates high enough to overwhelm selection (i.e., homogenizing dispersal). We used an aggregate measure of community fitness to infer a given community’s biogeochemical function relative to other communities. We also used ecological null models to further link the relative influence of deterministic assembly to function. We found that increasing rates of dispersal decrease biogeochemical function by increasing the proportion of maladapted taxa in a local community. Niche breadth was also a key determinant of biogeochemical function, suggesting a tradeoff between the function of generalist and specialist species. Finally, we show that microbial assembly processes exert greater influence over biogeochemical function whenmore » there is variation in the relative contributions of dispersal and selection among communities. Taken together, our results highlight the influence of spatial processes on biogeochemical function and indicate the need to account for such effects in models that aim to predict biogeochemical function under future environmental scenarios.« less

Authors:
ORCiD logo [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
Emily Graham; James Stegen
OSTI Identifier:
1415078
Report Number(s):
PNNL-SA-129385
Journal ID: ISSN 2227-9717; PROCCO; KP1702030
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Processes
Additional Journal Information:
Journal Volume: 5; Journal Issue: 4; Journal ID: ISSN 2227-9717
Publisher:
Multidisciplinary Digital Publishing Institute (MDPI)
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES; 54 ENVIRONMENTAL SCIENCES; stochasticity; determinism; microbial ecology; biogeochemistry; null model; ecosytem function

Citation Formats

Graham, Emily B., and Stegen, James C. Dispersal-Based Microbial Community Assembly Decreases Biogeochemical Function. United States: N. p., 2017. Web. doi:10.3390/pr5040065.
Graham, Emily B., & Stegen, James C. Dispersal-Based Microbial Community Assembly Decreases Biogeochemical Function. United States. doi:10.3390/pr5040065.
Graham, Emily B., and Stegen, James C. Wed . "Dispersal-Based Microbial Community Assembly Decreases Biogeochemical Function". United States. doi:10.3390/pr5040065. https://www.osti.gov/servlets/purl/1415078.
@article{osti_1415078,
title = {Dispersal-Based Microbial Community Assembly Decreases Biogeochemical Function},
author = {Graham, Emily B. and Stegen, James C.},
abstractNote = {Ecological mechanisms influence relationships among microbial communities, which in turn impact biogeochemistry. In particular, microbial communities are assembled by deterministic (e.g., selection) and stochastic (e.g., dispersal) processes, and the relative balance of these two process types is hypothesized to alter the influence of microbial communities over biogeochemical function. We used an ecological simulation model to evaluate this hypothesis, defining biogeochemical function generically to represent any biogeochemical reaction of interest. We assembled receiving communities under different levels of dispersal from a source community that was assembled purely by selection. The dispersal scenarios ranged from no dispersal (i.e., selection-only) to dispersal rates high enough to overwhelm selection (i.e., homogenizing dispersal). We used an aggregate measure of community fitness to infer a given community’s biogeochemical function relative to other communities. We also used ecological null models to further link the relative influence of deterministic assembly to function. We found that increasing rates of dispersal decrease biogeochemical function by increasing the proportion of maladapted taxa in a local community. Niche breadth was also a key determinant of biogeochemical function, suggesting a tradeoff between the function of generalist and specialist species. Finally, we show that microbial assembly processes exert greater influence over biogeochemical function when there is variation in the relative contributions of dispersal and selection among communities. Taken together, our results highlight the influence of spatial processes on biogeochemical function and indicate the need to account for such effects in models that aim to predict biogeochemical function under future environmental scenarios.},
doi = {10.3390/pr5040065},
journal = {Processes},
number = 4,
volume = 5,
place = {United States},
year = {2017},
month = {11}
}

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Works referenced in this record:

Bacterial carbon processing by generalist species in the coastal ocean
journal, January 2008

  • Mou, Xiaozhen; Sun, Shulei; Edwards, Robert A.
  • Nature, Vol. 451, Issue 7179
  • DOI: 10.1038/nature06513

Biological Determinants of Species Diversity
journal, January 1985

  • Shmida, Avi; Wilson, Mark V.
  • Journal of Biogeography, Vol. 12, Issue 1
  • DOI: 10.2307/2845026

Choosing and using diversity indices: insights for ecological applications from the German Biodiversity Exploratories
journal, August 2014

  • Morris, E. Kathryn; Caruso, Tancredi; Buscot, François
  • Ecology and Evolution, Vol. 4, Issue 18
  • DOI: 10.1002/ece3.1155

Biodiversity improves water quality through niche partitioning
journal, April 2011


Estimating and mapping ecological processes influencing microbial community assembly
journal, May 2015


Microbial community assembly, theory and rare functions
journal, January 2013

  • Pholchan, Mujalin K.; Baptista, Joana de C.; Davenport, Russell J.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00068

Historical Contingency in Community Assembly: Integrating Niches, Species Pools, and Priority Effects
journal, December 2015


The functional role of producer diversity in ecosystems
journal, March 2011

  • Cardinale, Bradley J.; Matulich, Kristin L.; Hooper, David U.
  • American Journal of Botany, Vol. 98, Issue 3
  • DOI: 10.3732/ajb.1000364

Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Coupling Spatiotemporal Community Assembly Processes to Changes in Microbial Metabolism
journal, December 2016


Climate and nitrogen controls on the geography and timescales of terrestrial biogeochemical cycling
journal, December 1996

  • Schimel, D. S.; Braswell, B. H.; McKeown, R.
  • Global Biogeochemical Cycles, Vol. 10, Issue 4
  • DOI: 10.1029/96GB01524

Weak coupling between community composition and functioning of aquatic bacteria
journal, May 2005

  • Langenheder, Silke; Lindström, Eva S.; Tranvik, Lars J.
  • Limnology and Oceanography, Vol. 50, Issue 3
  • DOI: 10.4319/lo.2005.50.3.0957

Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?
journal, February 2016

  • Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00214

A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning
journal, September 2011


Bacterial Biodiversity-Ecosystem Functioning Relations Are Modified by Environmental Complexity
journal, May 2010


Deterministic influences exceed dispersal effects on hydrologically-connected microbiomes: Deterministic assembly of hyporheic microbiomes
journal, March 2017

  • Graham, Emily B.; Crump, Alex R.; Resch, Charles T.
  • Environmental Microbiology, Vol. 19, Issue 4
  • DOI: 10.1111/1462-2920.13720

Autogenic succession and deterministic recovery following disturbance in soil bacterial communities
journal, April 2017

  • Jurburg, Stephanie D.; Nunes, Inês; Stegen, James C.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep45691

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


The contribution of species richness and composition to bacterial services
journal, August 2005

  • Bell, Thomas; Newman, Jonathan A.; Silverman, Bernard W.
  • Nature, Vol. 436, Issue 7054
  • DOI: 10.1038/nature03891

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

Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes
journal, February 2013


When should species richness be energy limited, and how would we know?
journal, January 2014

  • Hurlbert, Allen H.; Stegen, James C.
  • Ecology Letters, Vol. 17, Issue 4
  • DOI: 10.1111/ele.12240

Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem
journal, September 2016

  • Veach, Allison M.; Stegen, James C.; Brown, Shawn P.
  • Molecular Ecology, Vol. 25, Issue 18
  • DOI: 10.1111/mec.13784

Stochastic and deterministic assembly processes in subsurface microbial communities
journal, March 2012

  • Stegen, James C.; Lin, Xueju; Konopka, Allan E.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.22

Inferring Ecological Processes from Taxonomic, Phylogenetic and Functional Trait β-Diversity
journal, June 2011


A global synthesis reveals biodiversity loss as a major driver of ecosystem change
journal, May 2012

  • Hooper, David U.; Adair, E. Carol; Cardinale, Bradley J.
  • Nature, Vol. 486, Issue 7401
  • DOI: 10.1038/nature11118

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

Conceptual Synthesis in Community Ecology
journal, June 2010

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

Sources, Sinks, and Population Regulation
journal, November 1988

  • Pulliam, H. Ronald
  • The American Naturalist, Vol. 132, Issue 5
  • DOI: 10.1086/284880

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

Diversity and Productivity in a Long-Term Grassland Experiment
journal, October 2001


Mapping the niche space of soil microorganisms using taxonomy and traits
journal, August 2012

  • Lennon, Jay T.; Aanderud, Zachary T.; Lehmkuhl, B. K.
  • Ecology, Vol. 93, Issue 8
  • DOI: 10.1890/11-1745.1

The metacommunity concept: a framework for multi-scale community ecology: The metacommunity concept
journal, June 2004


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

Microbial communities acclimate to recurring changes in soil redox potential status: Fluctuating redox microbial communities
journal, December 2010


Changes in community assembly may shift the relationship between biodiversity and ecosystem function
journal, August 2014


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

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 dormancy improves development and experimental validation of ecosystem model
journal, July 2014

  • Wang, Gangsheng; Jagadamma, Sindhu; Mayes, Melanie A.
  • The ISME Journal, Vol. 9, Issue 1
  • DOI: 10.1038/ismej.2014.120

Representing life in the Earth system with soil microbial functional traits in the MIMICS model
journal, January 2015

  • Wieder, W. R.; Grandy, A. S.; Kallenbach, C. M.
  • Geoscientific Model Development, Vol. 8, Issue 6
  • DOI: 10.5194/gmd-8-1789-2015

Should Environmental Filtering be Abandoned?
journal, June 2017


Impacts of plant diversity on biomass production increase through time because of species complementarity
journal, November 2007

  • Cardinale, B. J.; Wright, J. P.; Cadotte, M. W.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 46
  • DOI: 10.1073/pnas.0709069104

Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern
journal, June 2002


Phylocom: software for the analysis of phylogenetic community structure and trait evolution
journal, August 2008


Linking microbial community structure and microbial processes: an empirical and conceptual overview
journal, September 2015

  • Bier, Raven L.; Bernhardt, Emily S.; Boot, Claudia M.
  • FEMS Microbiology Ecology, Vol. 91, Issue 10
  • DOI: 10.1093/femsec/fiv113

Response of the Soil Microbial Community to Changes in Precipitation in a Semiarid Ecosystem
journal, September 2012

  • Cregger, Melissa A.; Schadt, Christopher W.; McDowell, Nate G.
  • Applied and Environmental Microbiology, Vol. 78, Issue 24
  • DOI: 10.1128/AEM.02050-12

Diversity in Tropical Rain Forests and Coral Reefs
journal, March 1978


Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014


When, where and how does microbial community composition matter?
journal, September 2014


Quantifying community assembly processes and identifying features that impose them
journal, June 2013

  • Stegen, James C.; Lin, Xueju; Fredrickson, Jim K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.93

The Ecological Consequences of Changes in Biodiversity: A Search for General Principles
journal, July 1999


Beyond species: functional diversity and the maintenance of ecological processes and services: Functional diversity in ecology and conservation
journal, August 2011


Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed
journal, December 2014

  • Rocca, Jennifer D.; Hall, Edward K.; Lennon, Jay T.
  • The ISME Journal, Vol. 9, Issue 8
  • DOI: 10.1038/ismej.2014.252

Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses
journal, January 2013

  • Wang, Gangsheng; Post, Wilfred M.; Mayes, Melanie A.
  • Ecological Applications, Vol. 23, Issue 1
  • DOI: 10.1890/12-0681.1

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Diversity and Evenness: A Unifying Notation and Its Consequences
journal, March 1973


Groundwater–surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover
journal, April 2016

  • Stegen, James C.; Fredrickson, James K.; Wilkins, Michael J.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms11237

Applying population and community ecology theory to advance understanding of belowground biogeochemistry
journal, January 2017

  • Buchkowski, Robert W.; Bradford, Mark A.; Grandy, Andrew Stuart
  • Ecology Letters, Vol. 20, Issue 2
  • DOI: 10.1111/ele.12712

Spatial scaling of microbial biodiversity
journal, September 2006


On the Coexistence of Specialists and Generalists
journal, October 1994

  • Wilson, David Sloan; Yoshimura, Jin
  • The American Naturalist, Vol. 144, Issue 4
  • DOI: 10.1086/285702

Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments
journal, February 2010

  • Hollister, Emily B.; Engledow, Amanda S.; Hammett, Amy Jo M.
  • The ISME Journal, Vol. 4, Issue 6
  • DOI: 10.1038/ismej.2010.3

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


Agriculture's impact on microbial diversity and associated fluxes of carbon dioxide and methane
journal, April 2011

  • Levine, Uri Y.; Teal, Tracy K.; Robertson, G. Philip
  • The ISME Journal, Vol. 5, Issue 10
  • DOI: 10.1038/ismej.2011.40