Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance

Abstract Background Microbe-microbe interactions between members of the plant rhizosphere are important but remain poorly understood. A more comprehensive understanding of the molecular mechanisms used by microbes to cooperate, compete, and persist has been challenging because of the complexity of n...

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Autores principales:	Him K. Shrestha, Manasa R. Appidi, Manuel I. Villalobos Solis, Jia Wang, Dana L. Carper, Leah Burdick, Dale A. Pelletier, Mitchel J. Doktycz, Robert L. Hettich, Paul E. Abraham
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Rhizospheric microbiome Microbial consortia Defined community Reductionist approach Metaproteomics PTMs Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c9f668f12b134dbe8ff75a9c0e50d72a
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spelling	oai:doaj.org-article:c9f668f12b134dbe8ff75a9c0e50d72a2021-11-14T12:08:49ZMetaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance10.1186/s12866-021-02370-41471-2180https://doaj.org/article/c9f668f12b134dbe8ff75a9c0e50d72a2021-11-01T00:00:00Zhttps://doi.org/10.1186/s12866-021-02370-4https://doaj.org/toc/1471-2180Abstract Background Microbe-microbe interactions between members of the plant rhizosphere are important but remain poorly understood. A more comprehensive understanding of the molecular mechanisms used by microbes to cooperate, compete, and persist has been challenging because of the complexity of natural ecosystems and the limited control over environmental factors. One strategy to address this challenge relies on studying complexity in a progressive manner, by first building a detailed understanding of relatively simple subsets of the community and then achieving high predictive power through combining different building blocks (e.g., hosts, community members) for different environments. Herein, we coupled this reductionist approach with high-resolution mass spectrometry-based metaproteomics to study molecular mechanisms driving community assembly, adaptation, and functionality for a defined community of ten taxonomically diverse bacterial members of Populus deltoides rhizosphere co-cultured either in a complex or defined medium. Results Metaproteomics showed this defined community assembled into distinct microbiomes based on growth media that eventually exhibit composition and functional stability over time. The community grown in two different media showed variation in composition, yet both were dominated by only a few microbial strains. Proteome-wide interrogation provided detailed insights into the functional behavior of each dominant member as they adjust to changing community compositions and environments. The emergence and persistence of select microbes in these communities were driven by specialization in strategies including motility, antibiotic production, altered metabolism, and dormancy. Protein-level interrogation identified post-translational modifications that provided additional insights into regulatory mechanisms influencing microbial adaptation in the changing environments. Conclusions This study provides high-resolution proteome-level insights into our understanding of microbe-microbe interactions and highlights specialized biological processes carried out by specific members of assembled microbiomes to compete and persist in changing environmental conditions. Emergent properties observed in these lower complexity communities can then be re-evaluated as more complex systems are studied and, when a particular property becomes less relevant, higher-order interactions can be identified.Him K. ShresthaManasa R. AppidiManuel I. Villalobos SolisJia WangDana L. CarperLeah BurdickDale A. PelletierMitchel J. DoktyczRobert L. HettichPaul E. AbrahamBMCarticleRhizospheric microbiomeMicrobial consortiaDefined communityReductionist approachMetaproteomicsPTMsMicrobiologyQR1-502ENBMC Microbiology, Vol 21, Iss 1, Pp 1-17 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Rhizospheric microbiome Microbial consortia Defined community Reductionist approach Metaproteomics PTMs Microbiology QR1-502
spellingShingle	Rhizospheric microbiome Microbial consortia Defined community Reductionist approach Metaproteomics PTMs Microbiology QR1-502 Him K. Shrestha Manasa R. Appidi Manuel I. Villalobos Solis Jia Wang Dana L. Carper Leah Burdick Dale A. Pelletier Mitchel J. Doktycz Robert L. Hettich Paul E. Abraham Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
description	Abstract Background Microbe-microbe interactions between members of the plant rhizosphere are important but remain poorly understood. A more comprehensive understanding of the molecular mechanisms used by microbes to cooperate, compete, and persist has been challenging because of the complexity of natural ecosystems and the limited control over environmental factors. One strategy to address this challenge relies on studying complexity in a progressive manner, by first building a detailed understanding of relatively simple subsets of the community and then achieving high predictive power through combining different building blocks (e.g., hosts, community members) for different environments. Herein, we coupled this reductionist approach with high-resolution mass spectrometry-based metaproteomics to study molecular mechanisms driving community assembly, adaptation, and functionality for a defined community of ten taxonomically diverse bacterial members of Populus deltoides rhizosphere co-cultured either in a complex or defined medium. Results Metaproteomics showed this defined community assembled into distinct microbiomes based on growth media that eventually exhibit composition and functional stability over time. The community grown in two different media showed variation in composition, yet both were dominated by only a few microbial strains. Proteome-wide interrogation provided detailed insights into the functional behavior of each dominant member as they adjust to changing community compositions and environments. The emergence and persistence of select microbes in these communities were driven by specialization in strategies including motility, antibiotic production, altered metabolism, and dormancy. Protein-level interrogation identified post-translational modifications that provided additional insights into regulatory mechanisms influencing microbial adaptation in the changing environments. Conclusions This study provides high-resolution proteome-level insights into our understanding of microbe-microbe interactions and highlights specialized biological processes carried out by specific members of assembled microbiomes to compete and persist in changing environmental conditions. Emergent properties observed in these lower complexity communities can then be re-evaluated as more complex systems are studied and, when a particular property becomes less relevant, higher-order interactions can be identified.
format	article
author	Him K. Shrestha Manasa R. Appidi Manuel I. Villalobos Solis Jia Wang Dana L. Carper Leah Burdick Dale A. Pelletier Mitchel J. Doktycz Robert L. Hettich Paul E. Abraham
author_facet	Him K. Shrestha Manasa R. Appidi Manuel I. Villalobos Solis Jia Wang Dana L. Carper Leah Burdick Dale A. Pelletier Mitchel J. Doktycz Robert L. Hettich Paul E. Abraham
author_sort	Him K. Shrestha
title	Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
title_short	Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
title_full	Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
title_fullStr	Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
title_full_unstemmed	Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
title_sort	metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance
publisher	BMC
publishDate	2021
url	https://doaj.org/article/c9f668f12b134dbe8ff75a9c0e50d72a
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Metaproteomics reveals insights into microbial structure, interactions, and dynamic regulation in defined communities as they respond to environmental disturbance

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