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Title: Impacts of chemical gradients on microbial community structure

Abstract

Succession of redox processes is sometimes assumed to define a basic microbial community structure for ecosystems with oxygen gradients. In this paradigm, aerobic respiration, denitrification, fermentation and sulfate reduction proceed in a thermodynamically determined order, known as the ‘redox tower’. Here, we investigated whether redox sorting of microbial processes explains microbial community structure at low-oxygen concentrations. We subjected a diverse microbial community sampled from a coastal marine sediment to 100 days of tidal cycling in a laboratory chemostat. Oxygen gradients (both in space and time) led to the assembly of a microbial community dominated by populations that each performed aerobic and anaerobic metabolism in parallel. This was shown by metagenomics, transcriptomics, proteomics and stable isotope incubations. Effective oxygen consumption combined with the formation of microaggregates sustained the activity of oxygen-sensitive anaerobic enzymes, leading to braiding of unsorted redox processes, within and between populations. Analyses of available metagenomic data sets indicated that the same ecological strategies might also be successful in some natural ecosystems.

Authors:
 [1];  [2];  [3];  [4]; ORCiD logo [5];  [1];  [2];  [6];  [2];  [7];  [8];  [9]
  1. Univ. of Calgary, AB (Canada). Dept. of Geoscience; Max Planck Inst. for Marine Microbiology, Bremen (Germany)
  2. Max Planck Inst. for Marine Microbiology, Bremen (Germany)
  3. Max Planck Inst. for Marine Microbiology, Bremen (Germany); Bielefeld Univ. (Germany). Inst. for Genome Research and Systems Biology. Center for Biotechnology
  4. Bielefeld Univ. (Germany). Inst. for Genome Research and Systems Biology. Center for Biotechnology
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Science Division; Univ. of Tennessee, Knoxville, TN (United States). UT-ORNL Graduate School of Genome Science and Technology; The Moffitt Cancer Center and Research Inst., Tampa, FL (United States). Dept. of Molecular Oncology
  6. Max Planck Inst. for Marine Microbiology, Bremen (Germany); Univ. of Southern Denmark, Odense (Denmark). Nordic Center for Earth Evolution
  7. Max Planck Inst. for Marine Microbiology, Bremen (Germany). NIOZ Royal Netherlands Inst. for Sea Research, Yerseke (Netherlands)
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Science Division; Univ. of Tennessee, Knoxville, TN (United States). UT-ORNL Graduate School of Genome Science and Technology
  9. Univ. of Calgary, AB (Canada). Dept. of Geoscience; Max Planck Inst. for Marine Microbiology, Bremen (Germany); Bielefeld Univ. (Germany). Inst. for Genome Research and Systems Biology. Center for Biotechnology
Publication Date:
Research Org.:
Univ. of Calgary, AB (Canada); Max Planck Inst. for Marine Microbiology, Bremen (Germany); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; Natural Sciences and Engineering Research Council of Canada (NSERC); European Research Council (ERC); German Federal State North Rhine-Westphalia; Max Planck Society (Germany)
OSTI Identifier:
1394612
Grant/Contract Number:
AC05-00OR22725; MASEM 242635; StG 306933
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 11; Journal Issue: 4; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Chen, Jianwei, Hanke, Anna, Tegetmeyer, Halina E., Kattelmann, Ines, Sharma, Ritin, Hamann, Emmo, Hargesheimer, Theresa, Kraft, Beate, Lenk, Sabine, Geelhoed, Jeanine S., Hettich, Robert L., and Strous, Marc. Impacts of chemical gradients on microbial community structure. United States: N. p., 2017. Web. doi:10.1038/ismej.2016.175.
Chen, Jianwei, Hanke, Anna, Tegetmeyer, Halina E., Kattelmann, Ines, Sharma, Ritin, Hamann, Emmo, Hargesheimer, Theresa, Kraft, Beate, Lenk, Sabine, Geelhoed, Jeanine S., Hettich, Robert L., & Strous, Marc. Impacts of chemical gradients on microbial community structure. United States. doi:10.1038/ismej.2016.175.
Chen, Jianwei, Hanke, Anna, Tegetmeyer, Halina E., Kattelmann, Ines, Sharma, Ritin, Hamann, Emmo, Hargesheimer, Theresa, Kraft, Beate, Lenk, Sabine, Geelhoed, Jeanine S., Hettich, Robert L., and Strous, Marc. Tue . "Impacts of chemical gradients on microbial community structure". United States. doi:10.1038/ismej.2016.175. https://www.osti.gov/servlets/purl/1394612.
@article{osti_1394612,
title = {Impacts of chemical gradients on microbial community structure},
author = {Chen, Jianwei and Hanke, Anna and Tegetmeyer, Halina E. and Kattelmann, Ines and Sharma, Ritin and Hamann, Emmo and Hargesheimer, Theresa and Kraft, Beate and Lenk, Sabine and Geelhoed, Jeanine S. and Hettich, Robert L. and Strous, Marc},
abstractNote = {Succession of redox processes is sometimes assumed to define a basic microbial community structure for ecosystems with oxygen gradients. In this paradigm, aerobic respiration, denitrification, fermentation and sulfate reduction proceed in a thermodynamically determined order, known as the ‘redox tower’. Here, we investigated whether redox sorting of microbial processes explains microbial community structure at low-oxygen concentrations. We subjected a diverse microbial community sampled from a coastal marine sediment to 100 days of tidal cycling in a laboratory chemostat. Oxygen gradients (both in space and time) led to the assembly of a microbial community dominated by populations that each performed aerobic and anaerobic metabolism in parallel. This was shown by metagenomics, transcriptomics, proteomics and stable isotope incubations. Effective oxygen consumption combined with the formation of microaggregates sustained the activity of oxygen-sensitive anaerobic enzymes, leading to braiding of unsorted redox processes, within and between populations. Analyses of available metagenomic data sets indicated that the same ecological strategies might also be successful in some natural ecosystems.},
doi = {10.1038/ismej.2016.175},
journal = {The ISME Journal},
number = 4,
volume = 11,
place = {United States},
year = {Tue Jan 17 00:00:00 EST 2017},
month = {Tue Jan 17 00:00:00 EST 2017}
}

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