Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure...

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Autores principales:	Michaeline B. N. Albright, Sanna Sevanto, La Verne Gallegos-Graves, John Dunbar
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	microbiome engineering probiotics ecosystem manipulation invasion biology bacterial traits ecosystem functioning Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b9cf66b2d4324aac802e4c3fb3f838e0
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spelling	oai:doaj.org-article:b9cf66b2d4324aac802e4c3fb3f838e02021-11-15T16:19:08ZBiotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions10.1128/mBio.02089-202150-7511https://doaj.org/article/b9cf66b2d4324aac802e4c3fb3f838e02020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02089-20https://doaj.org/toc/2150-7511ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).Michaeline B. N. AlbrightSanna SevantoLa Verne Gallegos-GravesJohn DunbarAmerican Society for Microbiologyarticlemicrobiome engineeringprobioticsecosystem manipulationinvasion biologybacterial traitsecosystem functioningMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiome engineering probiotics ecosystem manipulation invasion biology bacterial traits ecosystem functioning Microbiology QR1-502
spellingShingle	microbiome engineering probiotics ecosystem manipulation invasion biology bacterial traits ecosystem functioning Microbiology QR1-502 Michaeline B. N. Albright Sanna Sevanto La Verne Gallegos-Graves John Dunbar Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
description	ABSTRACT Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).
format	article
author	Michaeline B. N. Albright Sanna Sevanto La Verne Gallegos-Graves John Dunbar
author_facet	Michaeline B. N. Albright Sanna Sevanto La Verne Gallegos-Graves John Dunbar
author_sort	Michaeline B. N. Albright
title	Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
title_short	Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
title_full	Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
title_fullStr	Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
title_full_unstemmed	Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions
title_sort	biotic interactions are more important than propagule pressure in microbial community invasions
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/b9cf66b2d4324aac802e4c3fb3f838e0
work_keys_str_mv	AT michaelinebnalbright bioticinteractionsaremoreimportantthanpropagulepressureinmicrobialcommunityinvasions AT sannasevanto bioticinteractionsaremoreimportantthanpropagulepressureinmicrobialcommunityinvasions AT lavernegallegosgraves bioticinteractionsaremoreimportantthanpropagulepressureinmicrobialcommunityinvasions AT johndunbar bioticinteractionsaremoreimportantthanpropagulepressureinmicrobialcommunityinvasions
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Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

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