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

Title: Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long‐term chronosequence

Abstract

Summary Soil microbial communities are abundant, hyper‐diverse and mediate global biogeochemical cycles, but we do not yet understand the processes mediating their assembly. Current hypothetical frameworks suggest temporal (e.g. dispersal limitation) and environmental (e.g. soil pH ) filters shape microbial community composition; however, there is limited empirical evidence supporting this framework in the hyper‐diverse soil environment, particularly at large spatial (i.e. regional to continental) and temporal (i.e. 100 to 1000 years) scales. Here, we present evidence from a long‐term chronosequence (4000 years) that temporal and environmental filters do indeed shape soil bacterial community composition. Furthermore, nearly 20 years of environmental monitoring allowed us to control for potentially confounding environmental variation. Soil bacterial communities were phylogenetically distinct across the chronosequence. We determined that temporal and environmental factors accounted for significant portions of bacterial phylogenetic structure using distance‐based linear models. Environmental factors together accounted for the majority of phylogenetic structure, namely, soil temperature (19%), pH (17%) and litter carbon:nitrogen (C:N; 17%). However, of all individual factors, time since deglaciation accounted for the greatest proportion of bacterial phylogenetic structure (20%). Taken together, our results provide empirical evidence that temporal and environmental filters act together to structure soil bacterial communities across large spatial andmore » long‐term temporal scales.« less

Authors:
 [1];  [2]
  1. School of Natural Resources &, Environment University of Michigan Ann Arbor MI 48109 USA
  2. School of Natural Resources &, Environment University of Michigan Ann Arbor MI 48109 USA, Department of Ecology and Evolution University of Michigan Ann Arbor MI 48109 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1464536
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Name: Environmental Microbiology Journal Volume: 17 Journal Issue: 9; Journal ID: ISSN 1462-2912
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Freedman, Zachary, and Zak, Donald R. Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long‐term chronosequence. United Kingdom: N. p., 2015. Web. doi:10.1111/1462-2920.12762.
Freedman, Zachary, & Zak, Donald R. Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long‐term chronosequence. United Kingdom. https://doi.org/10.1111/1462-2920.12762
Freedman, Zachary, and Zak, Donald R. Wed . "Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long‐term chronosequence". United Kingdom. https://doi.org/10.1111/1462-2920.12762.
@article{osti_1464536,
title = {Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long‐term chronosequence},
author = {Freedman, Zachary and Zak, Donald R.},
abstractNote = {Summary Soil microbial communities are abundant, hyper‐diverse and mediate global biogeochemical cycles, but we do not yet understand the processes mediating their assembly. Current hypothetical frameworks suggest temporal (e.g. dispersal limitation) and environmental (e.g. soil pH ) filters shape microbial community composition; however, there is limited empirical evidence supporting this framework in the hyper‐diverse soil environment, particularly at large spatial (i.e. regional to continental) and temporal (i.e. 100 to 1000 years) scales. Here, we present evidence from a long‐term chronosequence (4000 years) that temporal and environmental filters do indeed shape soil bacterial community composition. Furthermore, nearly 20 years of environmental monitoring allowed us to control for potentially confounding environmental variation. Soil bacterial communities were phylogenetically distinct across the chronosequence. We determined that temporal and environmental factors accounted for significant portions of bacterial phylogenetic structure using distance‐based linear models. Environmental factors together accounted for the majority of phylogenetic structure, namely, soil temperature (19%), pH (17%) and litter carbon:nitrogen (C:N; 17%). However, of all individual factors, time since deglaciation accounted for the greatest proportion of bacterial phylogenetic structure (20%). Taken together, our results provide empirical evidence that temporal and environmental filters act together to structure soil bacterial communities across large spatial and long‐term temporal scales.},
doi = {10.1111/1462-2920.12762},
journal = {Environmental Microbiology},
number = 9,
volume = 17,
place = {United Kingdom},
year = {Wed Feb 11 00:00:00 EST 2015},
month = {Wed Feb 11 00:00:00 EST 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1462-2920.12762

Citation Metrics:
Cited by: 72 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea
journal, August 2003


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 consequences of genetic drift for bacterial genome complexity
journal, June 2009


Assembly and response rules: two goals for predictive community ecology
journal, April 1992

  • Keddy, Paul A.
  • Journal of Vegetation Science, Vol. 3, Issue 2
  • DOI: 10.2307/3235676

Microbial biogeography: putting microorganisms on the map
journal, February 2006

  • Martiny, Jennifer B. Hughes; Bohannan, Brendan J. M.; Brown, James H.
  • Nature Reviews Microbiology, Vol. 4, Issue 2
  • DOI: 10.1038/nrmicro1341

Electrosynthesis of Commodity Chemicals by an Autotrophic Microbial Community
journal, September 2012

  • Marshall, Christopher W.; Ross, Daniel E.; Fichot, Erin B.
  • Applied and Environmental Microbiology, Vol. 78, Issue 23, p. 8412-8420
  • DOI: 10.1128/AEM.02401-12

Real-Time DNA Sequencing from Single Polymerase Molecules
journal, January 2009


Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield
journal, March 2012


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

Actinomycete-flora associated with submersed freshwater macrophytes
journal, June 1998


Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean
journal, October 2009

  • Schauer, Regina; Bienhold, Christina; Ramette, Alban
  • The ISME Journal, Vol. 4, Issue 2
  • DOI: 10.1038/ismej.2009.106

Use of multivariate methods in forest research site selection
journal, November 1991

  • Burton, Andrew J.; Ramm, Carl W.; Pregitzer, Kurt S.
  • Canadian Journal of Forest Research, Vol. 21, Issue 11
  • DOI: 10.1139/x91-219

Comparison of temperature effects on soil respiration and bacterial and fungal growth rates
journal, March 2005

  • PietikÃ¥inen, Janna; Pettersson, Marie; Bååth, Erland
  • FEMS Microbiology Ecology, Vol. 52, Issue 1
  • DOI: 10.1016/j.femsec.2004.10.002

Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives
journal, December 2013

  • Schlaeppi, K.; Dombrowski, N.; Oter, R. G.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
  • DOI: 10.1073/pnas.1321597111

Greatlakean Substage: A Replacement for Valderan Substage in the Lake Michigan Basin
journal, September 1976


Assembly history dictates ecosystem functioning: evidence from wood decomposer communities: Carbon dynamics and fungal community assembly
journal, April 2010


Conceptual Synthesis in Community Ecology
journal, June 2010

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

Dispersal limitation structures fungal community assembly in a long-term glacial chronosequence: Fungal community assembly
journal, October 2013


Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence : Actinobacterial Phylogeography
journal, February 2012

  • Eisenlord, Sarah D.; Zak, Donald R.; Upchurch, Rima A.
  • Ecology and Evolution, Vol. 2, Issue 3
  • DOI: 10.1002/ece3.210

The importance of physical isolation to microbial diversification
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

Rhizobium free-living nitrogen fixation occurs in specialized nongrowing cells
journal, March 1984


Degradation of lignin by bacteria
journal, February 1990


Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus
journal, April 2009


Microorganisms in the atmosphere over Antarctica: Microorganisms in the atmosphere over Antarctica
journal, August 2009


Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform
journal, March 2013


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

Atmospheric N Deposition Increases Bacterial Laccase-Like Multicopper Oxidases: Implications for Organic Matter Decay
journal, May 2014

  • Freedman, Zachary; Zak, Donald R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 14
  • DOI: 10.1128/AEM.01224-14

Variation in Forest Soil Properties along a Great Lakes Air Pollution Gradient
journal, January 1991


Inter-specific Interactions Between Carbon-limited Soil Bacteria Affect Behavior and Gene Expression
journal, March 2009


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

SIMULATED ATMOSPHERIC NO 3 DEPOSITION INCREASES SOIL ORGANIC MATTER BY SLOWING DECOMPOSITION
journal, December 2008

  • Zak, Donald R.; Holmes, William E.; Burton, Andrew J.
  • Ecological Applications, Vol. 18, Issue 8
  • DOI: 10.1890/07-1743.1

Isolation of bacterial strains able to metabolize lignin from screening of environmental samples
journal, June 2012


Microbial hitchhikers on intercontinental dust: catching a lift in Chad
journal, December 2012

  • Favet, Jocelyne; Lapanje, Ales; Giongo, Adriana
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.152

Two Invasive Plants Alter Soil Microbial Community Composition in Serpentine Grasslands
journal, March 2006


Quaternary History of Deciduous Forests of Eastern North America and Europe
journal, January 1983

  • Davis, Margaret B.
  • Annals of the Missouri Botanical Garden, Vol. 70, Issue 3
  • DOI: 10.2307/2992086

A flexible and efficient template format for circular consensus sequencing and SNP detection
journal, June 2010

  • Travers, K. J.; Chin, C. -S.; Rank, D. R.
  • Nucleic Acids Research, Vol. 38, Issue 15
  • DOI: 10.1093/nar/gkq543

The influence of soil properties on the structure of bacterial and fungal communities across land-use types
journal, September 2008

  • Lauber, Christian L.; Strickland, Michael S.; Bradford, Mark A.
  • Soil Biology and Biochemistry, Vol. 40, Issue 9
  • DOI: 10.1016/j.soilbio.2008.05.021

Succession of Bacterial Communities during Early Plant Development: Transition from Seed to Root and Effect of Compost Amendment
journal, June 2006

  • Green, S. J.; Inbar, E.; Michel, F. C.
  • Applied and Environmental Microbiology, Vol. 72, Issue 6
  • DOI: 10.1128/AEM.02771-05

Biogeography and Degree of Endemicity of Fluorescent Pseudomonas Strains in Soil
journal, December 2000


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

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

A general method applicable to the search for similarities in the amino acid sequence of two proteins
journal, March 1970


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

Role of Productivity and Protozoan Abundance for the Occurrence of Predation-resistant Bacteria in Aquatic Systems
journal, September 2007


A window into third-generation sequencing
journal, September 2010

  • Schadt, E. E.; Turner, S.; Kasarskis, A.
  • Human Molecular Genetics, Vol. 19, Issue R2
  • DOI: 10.1093/hmg/ddq416

Regional invariance among microbial communities
journal, January 2010


Soil Microbial Community Responses to Multiple Experimental Climate Change Drivers
journal, December 2009

  • Castro, H. F.; Classen, A. T.; Austin, E. E.
  • Applied and Environmental Microbiology, Vol. 76, Issue 4
  • DOI: 10.1128/AEM.02874-09

Towards a molecular understanding of N cycling in northern hardwood forests under future rates of N deposition
journal, November 2013


Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012


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

FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009

  • Price, M. N.; Dehal, P. S.; Arkin, A. P.
  • Molecular Biology and Evolution, Vol. 26, Issue 7
  • DOI: 10.1093/molbev/msp077

Biodiversity and Ecosystem Functioning: Current Knowledge and Future Challenges
journal, October 2001


Endemism and functional convergence across the North American soil mycobiome
journal, April 2014

  • Talbot, J. M.; Bruns, T. D.; Taylor, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1402584111

A method of linking multivariate community structure to environmental variables
journal, January 1993

  • Clarke, Kr; Ainsworth, M.
  • Marine Ecology Progress Series, Vol. 92
  • DOI: 10.3354/meps092205

Drivers of bacterial  -diversity depend on spatial scale
journal, April 2011

  • Martiny, J. B. H.; Eisen, J. A.; Penn, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 19
  • DOI: 10.1073/pnas.1016308108

UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems
journal, March 2008