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Title: Estimating taxon-specific population dynamics in diverse microbial communities

Abstract

Understanding how population-level dynamics contribute to ecosystem-level processes is a primary focus of ecological research and has led to important breakthroughs in the ecology of macroscopic organisms. However, the inability to measure population-specific rates, such as growth, for microbial taxa within natural assemblages has limited ecologists’ understanding of how microbial populations interact to regulate ecosystem processes. In this work, we use isotope incorporation within DNA molecules to model taxon-specific population growth in the presence of 18O-labeled water. By applying this model to phylogenetic marker sequencing data collected from stable-isotope probing studies, we estimate rates of growth, mortality, and turnover for individual microbial populations within soil assemblages. When summed across the entire bacterial community, our taxon-specific estimates are within the range of other whole-assemblage measurements of bacterial turnover. Because it can be applied to environmental samples, the approach we present is broadly applicable to measuring population growth, mortality, and associated biogeochemical process rates of microbial taxa for a wide range of ecosystems and can help reveal how individual microbial populations drive biogeochemical fluxes.

Authors:
 [1];  [1];  [1];  [2];  [3];  [2];  [1];  [2];  [1];  [4];  [3]; ORCiD logo [2]
  1. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff Arizona 86011 USA
  2. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff Arizona 86011 USA; Department of Biological Sciences, Northern Arizona University, Flagstaff Arizona 86011 USA
  3. Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore California 94550 USA
  4. Division of Plant and Soil Sciences, West Virginia University, Morgantown West Virginia 26506 USA
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Science Foundation (NSF); Technology Research Initiative Fund (TRIF)
OSTI Identifier:
1418693
Alternate Identifier(s):
OSTI ID: 1418696; OSTI ID: 1474397
Report Number(s):
LLNL-JRNL-731619; LLNL-JRNL-738626
Journal ID: ISSN 2150-8925; e02090
Grant/Contract Number:  
AC52-07NA27344; DEB‐1241094; DEB‐1146449; SC0016207; SCW1024; SCW1590
Resource Type:
Published Article
Journal Name:
Ecosphere
Additional Journal Information:
Journal Name: Ecosphere Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2150-8925
Publisher:
Ecological Society of America
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; population growth rate; population mortality rate; quantitative stable-isotope probing (qSIP); rewetting; soil bacteria; turnover

Citation Formats

Koch, Benjamin J., McHugh, Theresa A., Hayer, Michaela, Schwartz, Egbert, Blazewicz, Steven J., Dijkstra, Paul, van Gestel, Natasja, Marks, Jane C., Mau, Rebecca L., Morrissey, Ember M., Pett-Ridge, Jennifer, and Hungate, Bruce A. Estimating taxon-specific population dynamics in diverse microbial communities. United States: N. p., 2018. Web. doi:10.1002/ecs2.2090.
Koch, Benjamin J., McHugh, Theresa A., Hayer, Michaela, Schwartz, Egbert, Blazewicz, Steven J., Dijkstra, Paul, van Gestel, Natasja, Marks, Jane C., Mau, Rebecca L., Morrissey, Ember M., Pett-Ridge, Jennifer, & Hungate, Bruce A. Estimating taxon-specific population dynamics in diverse microbial communities. United States. https://doi.org/10.1002/ecs2.2090
Koch, Benjamin J., McHugh, Theresa A., Hayer, Michaela, Schwartz, Egbert, Blazewicz, Steven J., Dijkstra, Paul, van Gestel, Natasja, Marks, Jane C., Mau, Rebecca L., Morrissey, Ember M., Pett-Ridge, Jennifer, and Hungate, Bruce A. Mon . "Estimating taxon-specific population dynamics in diverse microbial communities". United States. https://doi.org/10.1002/ecs2.2090.
@article{osti_1418693,
title = {Estimating taxon-specific population dynamics in diverse microbial communities},
author = {Koch, Benjamin J. and McHugh, Theresa A. and Hayer, Michaela and Schwartz, Egbert and Blazewicz, Steven J. and Dijkstra, Paul and van Gestel, Natasja and Marks, Jane C. and Mau, Rebecca L. and Morrissey, Ember M. and Pett-Ridge, Jennifer and Hungate, Bruce A.},
abstractNote = {Understanding how population-level dynamics contribute to ecosystem-level processes is a primary focus of ecological research and has led to important breakthroughs in the ecology of macroscopic organisms. However, the inability to measure population-specific rates, such as growth, for microbial taxa within natural assemblages has limited ecologists’ understanding of how microbial populations interact to regulate ecosystem processes. In this work, we use isotope incorporation within DNA molecules to model taxon-specific population growth in the presence of 18O-labeled water. By applying this model to phylogenetic marker sequencing data collected from stable-isotope probing studies, we estimate rates of growth, mortality, and turnover for individual microbial populations within soil assemblages. When summed across the entire bacterial community, our taxon-specific estimates are within the range of other whole-assemblage measurements of bacterial turnover. Because it can be applied to environmental samples, the approach we present is broadly applicable to measuring population growth, mortality, and associated biogeochemical process rates of microbial taxa for a wide range of ecosystems and can help reveal how individual microbial populations drive biogeochemical fluxes.},
doi = {10.1002/ecs2.2090},
journal = {Ecosphere},
number = 1,
volume = 9,
place = {United States},
year = {Mon Jan 29 00:00:00 EST 2018},
month = {Mon Jan 29 00:00:00 EST 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1002/ecs2.2090

Citation Metrics:
Cited by: 55 works
Citation information provided by
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Figures / Tables:

Figure 1 Figure 1: A majority (74%) of the 326 prokaryotic genera present in the rewetted soil became enriched in 18O by the end of the 10-day incubation. The remaining 26% had excess atom fraction 18O values indistinguishable from zero and none had negative values, indicating that the qSIP method of estimatingmore » taxon-specific isotopic enrichment was robust against detecting false deviations from zero. Points are bootstrapped medians; bars are 90% confidence intervals. Colors denote different phyla and genera are ordered from highest enrichment to lowest enrichment within each phylum.« less

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