On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies

While the COVID-19 pandemic has led to increased focus on pathogenic microbes that cross the animal-human species barrier, calls to include non-pathogenic interactions in our perspective on public health are gaining traction in the academic community. Over generations, the diversity of the human gut...

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Autores principales:	Olaf F. A. Larsen, Linda H. M. van de Burgwal
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	transitions catastrophic collapse planetary health keystone taxa microbial guilds Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b4d295d312349e4babc395a68302954
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spelling	oai:doaj.org-article:5b4d295d312349e4babc395a683029542021-12-02T08:49:04ZOn the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies1664-302X10.3389/fmicb.2021.784797https://doaj.org/article/5b4d295d312349e4babc395a683029542021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.784797/fullhttps://doaj.org/toc/1664-302XWhile the COVID-19 pandemic has led to increased focus on pathogenic microbes that cross the animal-human species barrier, calls to include non-pathogenic interactions in our perspective on public health are gaining traction in the academic community. Over generations, the diversity of the human gut microbiota is being challenged by external perturbations and reduced acquisition of symbiotic species throughout life. When such reduced diversity concerns not only the microbial species, but also the higher taxonomic levels and even the guild level, adequate compensation for possible losses may be lacking. Shifts from a high-abundance to a low-abundance state, known as a tipping point, may result in simultaneous shifts in covarying taxa and ultimately to a catastrophic collapse in which the ecosystem abruptly and possibly irreversibly shifts to an alternative state. Here, we propose that co-occurrence patterns within and between microbial communities across human, animal, soil, water, and other environmental domains should be studied in light of such critical transitions. Improved mechanistic understanding of factors that shape structure and function is needed to understand whether interventions can sustainably remodel disease-prone microbiota compositions to robust and resilient healthy microbiota. Prerequisites for a rational approach are a better understanding of the microbial interaction network, both within and inter-domain, as well as the identification of early warning signs for a catastrophic collapse, warranting a timely response for intervention. We should not forget that mutualism and pathogenicity are two sides of the same coin. Building upon the planetary health concept, we argue that microbiome research should include system level approaches to conserve ecosystem resilience.HIGHLIGHTS1. Non-pathogenic interactions between ecosystems play a key role in maintaining health.2. The human gut microbiome may be on the verge of a catastrophic collapse.3. Research should identify keystone taxa and guilds that interconnect different domains.4. We should not forget that mutualism and pathogenicity are two sides of the same coin.Olaf F. A. LarsenLinda H. M. van de BurgwalFrontiers Media S.A.articletransitionscatastrophic collapseplanetary healthkeystone taxamicrobial guildsMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	transitions catastrophic collapse planetary health keystone taxa microbial guilds Microbiology QR1-502
spellingShingle	transitions catastrophic collapse planetary health keystone taxa microbial guilds Microbiology QR1-502 Olaf F. A. Larsen Linda H. M. van de Burgwal On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
description	While the COVID-19 pandemic has led to increased focus on pathogenic microbes that cross the animal-human species barrier, calls to include non-pathogenic interactions in our perspective on public health are gaining traction in the academic community. Over generations, the diversity of the human gut microbiota is being challenged by external perturbations and reduced acquisition of symbiotic species throughout life. When such reduced diversity concerns not only the microbial species, but also the higher taxonomic levels and even the guild level, adequate compensation for possible losses may be lacking. Shifts from a high-abundance to a low-abundance state, known as a tipping point, may result in simultaneous shifts in covarying taxa and ultimately to a catastrophic collapse in which the ecosystem abruptly and possibly irreversibly shifts to an alternative state. Here, we propose that co-occurrence patterns within and between microbial communities across human, animal, soil, water, and other environmental domains should be studied in light of such critical transitions. Improved mechanistic understanding of factors that shape structure and function is needed to understand whether interventions can sustainably remodel disease-prone microbiota compositions to robust and resilient healthy microbiota. Prerequisites for a rational approach are a better understanding of the microbial interaction network, both within and inter-domain, as well as the identification of early warning signs for a catastrophic collapse, warranting a timely response for intervention. We should not forget that mutualism and pathogenicity are two sides of the same coin. Building upon the planetary health concept, we argue that microbiome research should include system level approaches to conserve ecosystem resilience.HIGHLIGHTS1. Non-pathogenic interactions between ecosystems play a key role in maintaining health.2. The human gut microbiome may be on the verge of a catastrophic collapse.3. Research should identify keystone taxa and guilds that interconnect different domains.4. We should not forget that mutualism and pathogenicity are two sides of the same coin.
format	article
author	Olaf F. A. Larsen Linda H. M. van de Burgwal
author_facet	Olaf F. A. Larsen Linda H. M. van de Burgwal
author_sort	Olaf F. A. Larsen
title	On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
title_short	On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
title_full	On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
title_fullStr	On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
title_full_unstemmed	On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies
title_sort	on the verge of a catastrophic collapse? the need for a multi-ecosystem approach to microbiome studies
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/5b4d295d312349e4babc395a68302954
work_keys_str_mv	AT olaffalarsen onthevergeofacatastrophiccollapsetheneedforamultiecosystemapproachtomicrobiomestudies AT lindahmvandeburgwal onthevergeofacatastrophiccollapsetheneedforamultiecosystemapproachtomicrobiomestudies
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On the Verge of a Catastrophic Collapse? The Need for a Multi-Ecosystem Approach to Microbiome Studies

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