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Title: Evolutionary history constrains microbial traits across environmental variation

Abstract

Organisms influence ecosystems, from element cycling to disturbance regimes, to trophic interactions, to energy partitioning. Microorganisms are part of this influence, and understanding their ecology in nature requires studying traits of these organisms quantitatively in their natural habitats, a challenging task, but one which new approaches now make possible. Here, we show that growth rate and carbon assimilation rate of soil microorganisms are more influenced by evolutionary history than by climate, even across a broad climatic gradient spanning major temperate life zones, from mixed conifer forest to high desert grassland. Most of the explained variation (~50% to ~90%) in growth rate and carbon assimilation rate was attributable to difference among taxonomic groups indicating a strong influence of evolutionary history, and taxonomic groupings were more predictive for organisms responding to resource addition. With added carbon and nitrogen substrates, differences among taxonomic groups explained ~8 times more variance in growth rate than did the differences in ecosystem type. Taxon-specific growth and carbon assimilation rates were highly intercorrelated across the four ecosystems, constrained by the taxonomic identity of the organisms, such that plasticity driven by environment was limited across ecosystems varying in temperature, precipitation, and dominant vegetation. Taken together our results suggest that,more » similar to multicellular life, the traits of prokaryotes in their natural habitats are constrained by evolutionary history to a greater degree than environmental variation.« less

Authors:
ORCiD logo; ; ; ORCiD logo; ; ; ; ; ; ORCiD logo; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Northern Arizona Univ., Flagstaff, AZ (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Biological Systems Science Division; USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1557394
Alternate Identifier(s):
OSTI ID: 1557393; OSTI ID: 1567269
Report Number(s):
LLNL-JRNL-771085; PNNL-SA-147133
Journal ID: ISSN 2397-334X; 9285230925
Grant/Contract Number:  
SC0016207; AC52-07NA27344; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 3; Journal Issue: 7; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Morrissey, Ember M., Mau, Rebecca L., Hayer, Michaela, Liu, Xiao-Jun Allen, Schwartz, Egbert, Dijkstra, Paul, Koch, Benjamin J., Allen, Kara, Blazewicz, Steven J., Hofmockel, Kirsten, Pett-Ridge, Jennifer, and Hungate, Bruce A. Evolutionary history constrains microbial traits across environmental variation. United States: N. p., 2019. Web. doi:10.1038/s41559-019-0918-y.
Morrissey, Ember M., Mau, Rebecca L., Hayer, Michaela, Liu, Xiao-Jun Allen, Schwartz, Egbert, Dijkstra, Paul, Koch, Benjamin J., Allen, Kara, Blazewicz, Steven J., Hofmockel, Kirsten, Pett-Ridge, Jennifer, & Hungate, Bruce A. Evolutionary history constrains microbial traits across environmental variation. United States. doi:10.1038/s41559-019-0918-y.
Morrissey, Ember M., Mau, Rebecca L., Hayer, Michaela, Liu, Xiao-Jun Allen, Schwartz, Egbert, Dijkstra, Paul, Koch, Benjamin J., Allen, Kara, Blazewicz, Steven J., Hofmockel, Kirsten, Pett-Ridge, Jennifer, and Hungate, Bruce A. Mon . "Evolutionary history constrains microbial traits across environmental variation". United States. doi:10.1038/s41559-019-0918-y.
@article{osti_1557394,
title = {Evolutionary history constrains microbial traits across environmental variation},
author = {Morrissey, Ember M. and Mau, Rebecca L. and Hayer, Michaela and Liu, Xiao-Jun Allen and Schwartz, Egbert and Dijkstra, Paul and Koch, Benjamin J. and Allen, Kara and Blazewicz, Steven J. and Hofmockel, Kirsten and Pett-Ridge, Jennifer and Hungate, Bruce A.},
abstractNote = {Organisms influence ecosystems, from element cycling to disturbance regimes, to trophic interactions, to energy partitioning. Microorganisms are part of this influence, and understanding their ecology in nature requires studying traits of these organisms quantitatively in their natural habitats, a challenging task, but one which new approaches now make possible. Here, we show that growth rate and carbon assimilation rate of soil microorganisms are more influenced by evolutionary history than by climate, even across a broad climatic gradient spanning major temperate life zones, from mixed conifer forest to high desert grassland. Most of the explained variation (~50% to ~90%) in growth rate and carbon assimilation rate was attributable to difference among taxonomic groups indicating a strong influence of evolutionary history, and taxonomic groupings were more predictive for organisms responding to resource addition. With added carbon and nitrogen substrates, differences among taxonomic groups explained ~8 times more variance in growth rate than did the differences in ecosystem type. Taxon-specific growth and carbon assimilation rates were highly intercorrelated across the four ecosystems, constrained by the taxonomic identity of the organisms, such that plasticity driven by environment was limited across ecosystems varying in temperature, precipitation, and dominant vegetation. Taken together our results suggest that, similar to multicellular life, the traits of prokaryotes in their natural habitats are constrained by evolutionary history to a greater degree than environmental variation.},
doi = {10.1038/s41559-019-0918-y},
journal = {Nature Ecology and Evolution},
number = 7,
volume = 3,
place = {United States},
year = {2019},
month = {6}
}

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Works referenced in this record:

Horizontal gene transfer, genome innovation and evolution
journal, August 2005

  • Gogarten, J. Peter; Townsend, Jeffrey P.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1204

Are microbiome studies ready for hypothesis-driven research?
journal, August 2018

  • Tripathi, Anupriya; Marotz, Clarisse; Gonzalez, Antonio
  • Current Opinion in Microbiology, Vol. 44
  • DOI: 10.1016/j.mib.2018.07.002

Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model
journal, February 2003


How do traits vary across ecological scales? A case for trait-based ecology: How do traits vary across ecological scales?
journal, May 2010


PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009


Trait-based approaches for understanding microbial biodiversity and ecosystem functioning
journal, May 2014


Carbon flow in the rhizosphere: carbon trading at the soil–root interface
journal, February 2009


Taxonomic patterns in the nitrogen assimilation of soil prokaryotes: Nitrogen assimilation of soil prokaryotes
journal, March 2018

  • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
  • Environmental Microbiology, Vol. 20, Issue 3
  • DOI: 10.1111/1462-2920.14051

Predicting microbial traits with phylogenies
journal, September 2015


Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
journal, December 2012

  • Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
  • Nature Methods, Vol. 10, Issue 1
  • DOI: 10.1038/nmeth.2276

Rebuilding community ecology from functional traits
journal, April 2006


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


Examining variation in the leaf mass per area of dominant species across two contrasting tropical gradients in light of community assembly
journal, July 2016

  • Neyret, Margot; Bentley, Lisa Patrick; Oliveras, Imma
  • Ecology and Evolution, Vol. 6, Issue 16
  • DOI: 10.1002/ece3.2281

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

Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification
journal, September 2011

  • Berry, David; Ben Mahfoudh, Karim; Wagner, Michael
  • Applied and Environmental Microbiology, Vol. 77, Issue 21
  • DOI: 10.1128/AEM.05220-11

Functional trait variation along environmental gradients in temperate and Mediterranean trees: Functional trait variation in temperate and Mediterranean trees
journal, September 2015

  • Vilà-Cabrera, Albert; Martínez-Vilalta, Jordi; Retana, Javier
  • Global Ecology and Biogeography, Vol. 24, Issue 12
  • DOI: 10.1111/geb.12379

Phylogenetic organization of bacterial activity
journal, March 2016

  • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
  • The ISME Journal, Vol. 10, Issue 9
  • DOI: 10.1038/ismej.2016.28

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

The ecological coherence of high bacterial taxonomic ranks
journal, June 2010

  • Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J.
  • Nature Reviews Microbiology, Vol. 8, Issue 7
  • DOI: 10.1038/nrmicro2367

Inclusion of ecologically based trait variation in plant functional types reduces the projected land carbon sink in an earth system model
journal, March 2015

  • Verheijen, Lieneke M.; Aerts, Rien; Brovkin, Victor
  • Global Change Biology, Vol. 21, Issue 8
  • DOI: 10.1111/gcb.12871

Exploring Predictions of Abundance from Body Mass Using Hierarchical Comparative Approaches
journal, July 2008

  • McGill, Brian J.
  • The American Naturalist, Vol. 172, Issue 1
  • DOI: 10.1086/588044

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

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014

  • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
  • Nature Reviews Microbiology, Vol. 12, Issue 9
  • DOI: 10.1038/nrmicro3330

Response of Terrestrial CH4 Uptake to Interactive Changes in Precipitation and Temperature Along a Climatic Gradient
journal, October 2010


Revisiting life strategy concepts in environmental microbial ecology
journal, January 2017

  • Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E.
  • FEMS Microbiology Ecology
  • DOI: 10.1093/femsec/fix006

Water pulses and biogeochemical cycles in arid and semiarid ecosystems
journal, February 2004


Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction
journal, September 2016


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

Microbial hotspots and hot moments in soil: Concept & review
journal, April 2015


Quantitative Microbial Ecology through Stable Isotope Probing
journal, August 2015

  • Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert
  • Applied and Environmental Microbiology, Vol. 81, Issue 21
  • DOI: 10.1128/AEM.02280-15

Microbial Biogeography: From Taxonomy to Traits
journal, May 2008


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


Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter
journal, April 2017

  • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.43

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
journal, August 2015

  • Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
  • DOI: 10.1073/pnas.1508382112

Labile carbon input determines the direction and magnitude of the priming effect
journal, January 2017


Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations
journal, May 2017


Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California
journal, February 2009

  • Cornwell, William K.; Ackerly, David D.
  • Ecological Monographs, Vol. 79, Issue 1
  • DOI: 10.1890/07-1134.1

    Works referencing / citing this record:

    Examining variation in the leaf mass per area of dominant species across two contrasting tropical gradients in light of community assembly
    journal, July 2016

    • Neyret, Margot; Bentley, Lisa Patrick; Oliveras, Imma
    • Ecology and Evolution, Vol. 6, Issue 16
    • DOI: 10.1002/ece3.2281

    Water pulses and biogeochemical cycles in arid and semiarid ecosystems
    journal, February 2004


    Response of Terrestrial CH4 Uptake to Interactive Changes in Precipitation and Temperature Along a Climatic Gradient
    journal, October 2010


    Carbon flow in the rhizosphere: carbon trading at the soil–root interface
    journal, February 2009


    Labile carbon input determines the direction and magnitude of the priming effect
    journal, January 2017


    Are microbiome studies ready for hypothesis-driven research?
    journal, August 2018

    • Tripathi, Anupriya; Marotz, Clarisse; Gonzalez, Antonio
    • Current Opinion in Microbiology, Vol. 44
    • DOI: 10.1016/j.mib.2018.07.002

    Microbial hotspots and hot moments in soil: Concept & review
    journal, April 2015


    Rebuilding community ecology from functional traits
    journal, April 2006


    Phylogenetic conservatism of functional traits in microorganisms
    journal, December 2012

    • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
    • The ISME Journal, Vol. 7, Issue 4
    • DOI: 10.1038/ismej.2012.160

    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

    Predicting microbial traits with phylogenies
    journal, September 2015


    Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction
    journal, September 2016


    Phylogenetic organization of bacterial activity
    journal, March 2016

    • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
    • The ISME Journal, Vol. 10, Issue 9
    • DOI: 10.1038/ismej.2016.28

    Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter
    journal, April 2017

    • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
    • The ISME Journal, Vol. 11, Issue 8
    • DOI: 10.1038/ismej.2017.43

    Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations
    journal, May 2017


    Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
    journal, December 2012

    • Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
    • Nature Methods, Vol. 10, Issue 1
    • DOI: 10.1038/nmeth.2276

    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

    Horizontal gene transfer, genome innovation and evolution
    journal, August 2005

    • Gogarten, J. Peter; Townsend, Jeffrey P.
    • Nature Reviews Microbiology, Vol. 3, Issue 9
    • DOI: 10.1038/nrmicro1204

    The ecological coherence of high bacterial taxonomic ranks
    journal, June 2010

    • Philippot, Laurent; Andersson, Siv G. E.; Battin, Tom J.
    • Nature Reviews Microbiology, Vol. 8, Issue 7
    • DOI: 10.1038/nrmicro2367

    Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
    journal, August 2014

    • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
    • Nature Reviews Microbiology, Vol. 12, Issue 9
    • DOI: 10.1038/nrmicro3330

    Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model
    journal, February 2003


    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

    Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
    journal, August 2015

    • Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M.
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
    • DOI: 10.1073/pnas.1508382112

    Exploring Predictions of Abundance from Body Mass Using Hierarchical Comparative Approaches
    journal, July 2008

    • McGill, Brian J.
    • The American Naturalist, Vol. 172, Issue 1
    • DOI: 10.1086/588044

    PyNAST: a flexible tool for aligning sequences to a template alignment
    journal, November 2009


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


    Revisiting life strategy concepts in environmental microbial ecology
    journal, January 2017

    • Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E.
    • FEMS Microbiology Ecology
    • DOI: 10.1093/femsec/fix006

    Taxonomic patterns in the nitrogen assimilation of soil prokaryotes: Nitrogen assimilation of soil prokaryotes
    journal, March 2018

    • Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert
    • Environmental Microbiology, Vol. 20, Issue 3
    • DOI: 10.1111/1462-2920.14051

    Inclusion of ecologically based trait variation in plant functional types reduces the projected land carbon sink in an earth system model
    journal, March 2015

    • Verheijen, Lieneke M.; Aerts, Rien; Brovkin, Victor
    • Global Change Biology, Vol. 21, Issue 8
    • DOI: 10.1111/gcb.12871

    Functional trait variation along environmental gradients in temperate and Mediterranean trees: Functional trait variation in temperate and Mediterranean trees
    journal, September 2015

    • Vilà-Cabrera, Albert; Martínez-Vilalta, Jordi; Retana, Javier
    • Global Ecology and Biogeography, Vol. 24, Issue 12
    • DOI: 10.1111/geb.12379

    How do traits vary across ecological scales? A case for trait-based ecology: How do traits vary across ecological scales?
    journal, May 2010


    Microbial Biogeography: From Taxonomy to Traits
    journal, May 2008


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


    Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California
    journal, February 2009

    • Cornwell, William K.; Ackerly, David D.
    • Ecological Monographs, Vol. 79, Issue 1
    • DOI: 10.1890/07-1134.1

    Trait-based approaches for understanding microbial biodiversity and ecosystem functioning
    journal, May 2014


    Traits track taxonomy
    journal, June 2019