Visualizing Microbial Community Dynamics via a Controllable Soil Environment

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 rele...

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Autores principales:	Arunima Bhattacharjee, Dusan Velickovic, Thomas W. Wietsma, Sheryl L. Bell, Janet K. Jansson, Kirsten S. Hofmockel, Christopher R. Anderton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	SoilBox metaphenome mass spectrometry imaging chitin soil moisture fungal bridging Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/47bed323bd8047748e1b298c1b125025
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spelling	oai:doaj.org-article:47bed323bd8047748e1b298c1b1250252021-12-02T19:47:34ZVisualizing Microbial Community Dynamics via a Controllable Soil Environment10.1128/mSystems.00645-192379-5077https://doaj.org/article/47bed323bd8047748e1b298c1b1250252020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00645-19https://doaj.org/toc/2379-5077ABSTRACT 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.Arunima BhattacharjeeDusan VelickovicThomas W. WietsmaSheryl L. BellJanet K. JanssonKirsten S. HofmockelChristopher R. AndertonAmerican Society for MicrobiologyarticleSoilBoxmetaphenomemass spectrometry imagingchitinsoil moisturefungal bridgingMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	SoilBox metaphenome mass spectrometry imaging chitin soil moisture fungal bridging Microbiology QR1-502
spellingShingle	SoilBox metaphenome mass spectrometry imaging chitin soil moisture fungal bridging Microbiology QR1-502 Arunima Bhattacharjee Dusan Velickovic Thomas W. Wietsma Sheryl L. Bell Janet K. Jansson Kirsten S. Hofmockel Christopher R. Anderton Visualizing Microbial Community Dynamics via a Controllable Soil Environment
description	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.
format	article
author	Arunima Bhattacharjee Dusan Velickovic Thomas W. Wietsma Sheryl L. Bell Janet K. Jansson Kirsten S. Hofmockel Christopher R. Anderton
author_facet	Arunima Bhattacharjee Dusan Velickovic Thomas W. Wietsma Sheryl L. Bell Janet K. Jansson Kirsten S. Hofmockel Christopher R. Anderton
author_sort	Arunima Bhattacharjee
title	Visualizing Microbial Community Dynamics via a Controllable Soil Environment
title_short	Visualizing Microbial Community Dynamics via a Controllable Soil Environment
title_full	Visualizing Microbial Community Dynamics via a Controllable Soil Environment
title_fullStr	Visualizing Microbial Community Dynamics via a Controllable Soil Environment
title_full_unstemmed	Visualizing Microbial Community Dynamics via a Controllable Soil Environment
title_sort	visualizing microbial community dynamics via a controllable soil environment
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/47bed323bd8047748e1b298c1b125025
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Visualizing Microbial Community Dynamics via a Controllable Soil Environment

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