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Title: Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales

Abstract

Soils contain a tangle of minerals, water, nutrients, gases, plant roots, decaying organic matter, and microorganisms which work together to cycle nutrients and support terrestrial plant growth. Most soil microorganisms live in periodically interconnected communities closely associated with soil aggregates, i.e., small (<2 mm), strongly bound clusters of minerals and organic carbon that persist through mechanical disruptions and wetting events. Their spatial structure is important for biogeochemical cycling, and we cannot reliably predict soil biological activities and variability by studying bulk soils alone. To fully understand the biogeochemical processes at work in soils, it is necessary to understand the micrometer-scale interactions that occur between soil particles and their microbial inhabitants. Here, we review the current state of knowledge regarding soil aggregate microbial communities and identify areas of opportunity to study soil ecosystems at a scale relevant to individual cells. We present a framework for understanding aggregate communities as “microbial villages” that are periodically connected through wetting events, allowing for the transfer of genetic material, metabolites, and viruses. Here, we describe both top-down (whole community) and bottom-up (reductionist) strategies for studying these communities. Understanding this requires combining “model system” approaches (e.g., developing mock community artificial aggregates), field observations of natural communities,more » and broader study of community interactions to include understudied community members, like viruses. Initial studies suggest that aggregate-based approaches are a critical next step for developing a predictive understanding of how geochemical and community interactions govern microbial community structure and nutrient cycling in soil.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1];  [2]; ORCiD logo [1]; ORCiD logo [1];  [2]; ORCiD logo [1]; ORCiD logo [1];  [3]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. The Ohio State Univ., Columbus, OH (United States)
  3. Goethe Univ., Frankfurt am Main (Germany)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1542240
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 14; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; 54 ENVIRONMENTAL SCIENCES; microbial communities; soil; soil aggregate; virus

Citation Formats

Wilpiszeski, Regina L., Aufrecht, Jayde A., Retterer, Scott T., Sullivan, Matthew B., Graham, David E., Pierce, Eric M., Zablocki, Olivier D., Palumbo, Anthony V., Elias, Dwayne A., and Müller, Volker. Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales. United States: N. p., 2019. Web. doi:10.1128/AEM.00324-19.
Wilpiszeski, Regina L., Aufrecht, Jayde A., Retterer, Scott T., Sullivan, Matthew B., Graham, David E., Pierce, Eric M., Zablocki, Olivier D., Palumbo, Anthony V., Elias, Dwayne A., & Müller, Volker. Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales. United States. doi:10.1128/AEM.00324-19.
Wilpiszeski, Regina L., Aufrecht, Jayde A., Retterer, Scott T., Sullivan, Matthew B., Graham, David E., Pierce, Eric M., Zablocki, Olivier D., Palumbo, Anthony V., Elias, Dwayne A., and Müller, Volker. Fri . "Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales". United States. doi:10.1128/AEM.00324-19.
@article{osti_1542240,
title = {Soil Aggregate Microbial Communities: Towards Understanding Microbiome Interactions at Biologically Relevant Scales},
author = {Wilpiszeski, Regina L. and Aufrecht, Jayde A. and Retterer, Scott T. and Sullivan, Matthew B. and Graham, David E. and Pierce, Eric M. and Zablocki, Olivier D. and Palumbo, Anthony V. and Elias, Dwayne A. and Müller, Volker},
abstractNote = {Soils contain a tangle of minerals, water, nutrients, gases, plant roots, decaying organic matter, and microorganisms which work together to cycle nutrients and support terrestrial plant growth. Most soil microorganisms live in periodically interconnected communities closely associated with soil aggregates, i.e., small (<2 mm), strongly bound clusters of minerals and organic carbon that persist through mechanical disruptions and wetting events. Their spatial structure is important for biogeochemical cycling, and we cannot reliably predict soil biological activities and variability by studying bulk soils alone. To fully understand the biogeochemical processes at work in soils, it is necessary to understand the micrometer-scale interactions that occur between soil particles and their microbial inhabitants. Here, we review the current state of knowledge regarding soil aggregate microbial communities and identify areas of opportunity to study soil ecosystems at a scale relevant to individual cells. We present a framework for understanding aggregate communities as “microbial villages” that are periodically connected through wetting events, allowing for the transfer of genetic material, metabolites, and viruses. Here, we describe both top-down (whole community) and bottom-up (reductionist) strategies for studying these communities. Understanding this requires combining “model system” approaches (e.g., developing mock community artificial aggregates), field observations of natural communities, and broader study of community interactions to include understudied community members, like viruses. Initial studies suggest that aggregate-based approaches are a critical next step for developing a predictive understanding of how geochemical and community interactions govern microbial community structure and nutrient cycling in soil.},
doi = {10.1128/AEM.00324-19},
journal = {Applied and Environmental Microbiology},
number = 14,
volume = 85,
place = {United States},
year = {2019},
month = {5}
}

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Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O
journal, February 2007


Silicon Hyperuniform Disordered Photonic Materials with a Pronounced Gap in the Shortwave Infrared
journal, December 2013

  • Muller, Nicolas; Haberko, Jakub; Marichy, Catherine
  • Advanced Optical Materials, Vol. 2, Issue 2
  • DOI: 10.1002/adom.201300415

Elevated Abundance of Bacteriophage Infecting Bacteria in Soil
journal, January 2003


Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases
journal, January 2018


Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment
journal, September 2001