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Title: Visualizing Microbial Community Dynamics via a Controllable Soil Environment

Abstract

ABSTRACT Understanding the basic biology that underpins soil microbiome interactions is required to predict the metaphenomic response to environmental shifts. A significant knowledge gap remains in how such changes affect microbial community dynamics and their metabolic landscape at microbially relevant spatial scales. Using a custom-built SoilBox system, here we demonstrated changes in microbial community growth and composition in different soil environments (14%, 24%, and 34% soil moisture), contingent upon access to reservoirs of nutrient sources. The SoilBox emulates the probing depth of a common soil core and enables determination of both the spatial organization of the microbial communities and their metabolites, as shown by confocal microscopy in combination with mass spectrometry imaging (MSI). Using chitin as a nutrient source, we used the SoilBox system to observe increased adhesion of microbial biomass on chitin islands resulting in degradation of chitin into N -acetylglucosamine (NAG) and chitobiose. With matrix-assisted laser desorption/ionization (MALDI)-MSI, we also observed several phospholipid families that are functional biomarkers for microbial growth on the chitin islands. Fungal hyphal networks bridging different chitin islands over distances of 27 mm were observed only in the 14% soil moisture regime, indicating that such bridges may act as nutrient highways under drought conditions. Inmore » total, these results illustrate a system that can provide unprecedented spatial information about interactions within soil microbial communities as a function of changing environments. We anticipate that this platform will be invaluable in spatially probing specific intra- and interkingdom functional relationships of microbiomes within soil. IMPORTANCE Microbial communities are key components of the soil ecosystem. Recent advances in metagenomics and other omics capabilities have expanded our ability to characterize the composition and function of the soil microbiome. However, characterizing the spatial metabolic and morphological diversity of microbial communities remains a challenge due to the dynamic and complex nature of soil microenvironments. The SoilBox system, demonstrated in this work, simulates an ∼12-cm soil depth, similar to a typical soil core, and provides a platform that facilitates imaging the molecular and topographical landscape of soil microbial communities as a function of environmental gradients. Moreover, the nondestructive harvesting of soil microbial communities for the imaging experiments can enable simultaneous multiomics analysis throughout the depth of the SoilBox. Our results show that by correlating molecular and optical imaging data obtained using the SoilBox platform, deeper insights into the nature of specific soil microbial interactions can be achieved.« less

Authors:
; ; ; ; ; ; ORCiD logo;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1598721
Alternate Identifier(s):
OSTI ID: 1600533
Report Number(s):
PNNL-SA-147223
Journal ID: ISSN 2379-5077; e00645-19; /msystems/5/1/msys.00645-19.atom
Grant/Contract Number:  
Office of Biological and Environmental Research; AC05-76RL01830
Resource Type:
Published Article
Journal Name:
mSystems
Additional Journal Information:
Journal Name: mSystems Journal Volume: 5 Journal Issue: 1; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English

Citation Formats

Bhattacharjee, Arunima, Velickovic, Dusan, Wietsma, Thomas W., Bell, Sheryl L., Jansson, Janet K., Hofmockel, Kirsten S., Anderton, Christopher R., and Wilmes, ed., Paul. Visualizing Microbial Community Dynamics via a Controllable Soil Environment. United States: N. p., 2020. Web. doi:10.1128/mSystems.00645-19.
Bhattacharjee, Arunima, Velickovic, Dusan, Wietsma, Thomas W., Bell, Sheryl L., Jansson, Janet K., Hofmockel, Kirsten S., Anderton, Christopher R., & Wilmes, ed., Paul. Visualizing Microbial Community Dynamics via a Controllable Soil Environment. United States. doi:10.1128/mSystems.00645-19.
Bhattacharjee, Arunima, Velickovic, Dusan, Wietsma, Thomas W., Bell, Sheryl L., Jansson, Janet K., Hofmockel, Kirsten S., Anderton, Christopher R., and Wilmes, ed., Paul. Tue . "Visualizing Microbial Community Dynamics via a Controllable Soil Environment". United States. doi:10.1128/mSystems.00645-19.
@article{osti_1598721,
title = {Visualizing Microbial Community Dynamics via a Controllable Soil Environment},
author = {Bhattacharjee, Arunima and Velickovic, Dusan and Wietsma, Thomas W. and Bell, Sheryl L. and Jansson, Janet K. and Hofmockel, Kirsten S. and Anderton, Christopher R. and Wilmes, ed., Paul},
abstractNote = {ABSTRACT Understanding the basic biology that underpins soil microbiome interactions is required to predict the metaphenomic response to environmental shifts. A significant knowledge gap remains in how such changes affect microbial community dynamics and their metabolic landscape at microbially relevant spatial scales. Using a custom-built SoilBox system, here we demonstrated changes in microbial community growth and composition in different soil environments (14%, 24%, and 34% soil moisture), contingent upon access to reservoirs of nutrient sources. The SoilBox emulates the probing depth of a common soil core and enables determination of both the spatial organization of the microbial communities and their metabolites, as shown by confocal microscopy in combination with mass spectrometry imaging (MSI). Using chitin as a nutrient source, we used the SoilBox system to observe increased adhesion of microbial biomass on chitin islands resulting in degradation of chitin into N -acetylglucosamine (NAG) and chitobiose. With matrix-assisted laser desorption/ionization (MALDI)-MSI, we also observed several phospholipid families that are functional biomarkers for microbial growth on the chitin islands. Fungal hyphal networks bridging different chitin islands over distances of 27 mm were observed only in the 14% soil moisture regime, indicating that such bridges may act as nutrient highways under drought conditions. In total, these results illustrate a system that can provide unprecedented spatial information about interactions within soil microbial communities as a function of changing environments. We anticipate that this platform will be invaluable in spatially probing specific intra- and interkingdom functional relationships of microbiomes within soil. IMPORTANCE Microbial communities are key components of the soil ecosystem. Recent advances in metagenomics and other omics capabilities have expanded our ability to characterize the composition and function of the soil microbiome. However, characterizing the spatial metabolic and morphological diversity of microbial communities remains a challenge due to the dynamic and complex nature of soil microenvironments. The SoilBox system, demonstrated in this work, simulates an ∼12-cm soil depth, similar to a typical soil core, and provides a platform that facilitates imaging the molecular and topographical landscape of soil microbial communities as a function of environmental gradients. Moreover, the nondestructive harvesting of soil microbial communities for the imaging experiments can enable simultaneous multiomics analysis throughout the depth of the SoilBox. Our results show that by correlating molecular and optical imaging data obtained using the SoilBox platform, deeper insights into the nature of specific soil microbial interactions can be achieved.},
doi = {10.1128/mSystems.00645-19},
journal = {mSystems},
number = 1,
volume = 5,
place = {United States},
year = {2020},
month = {2}
}

Journal Article:
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DOI: 10.1128/mSystems.00645-19

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