Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

ABSTRACT The microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health, and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial c...

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Autores principales:	Deepika Sundarraman, Edouard A. Hay, Dylan M. Martins, Drew S. Shields, Noah L. Pettinari, Raghuveer Parthasarathy
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	gut microbiome microbial interactions zebrafish gnotobiotic Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dc5d529796de45a2bbd3310ea1ec123f
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spelling	oai:doaj.org-article:dc5d529796de45a2bbd3310ea1ec123f2021-11-15T16:19:08ZHigher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome10.1128/mBio.01667-202150-7511https://doaj.org/article/dc5d529796de45a2bbd3310ea1ec123f2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01667-20https://doaj.org/toc/2150-7511ABSTRACT The microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health, and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial composition remain largely unknown. Further, it is unclear for many multispecies consortia whether their species-level makeup can be predicted based on an understanding of pairwise species interactions or whether higher-order interactions are needed to explain emergent compositions. To address this, we examine commensal intestinal microbes in larval zebrafish, initially raised germfree, to allow the introduction of controlled combinations of bacterial species. Using a dissection and plating assay, we demonstrate the construction of communities of one to five bacterial species and show that the outcomes from the two-species competitions fail to predict species abundances in more complex communities. With multiple species present, interbacterial interactions become weaker, suggesting that higher-order interactions in the vertebrate gut stabilize complex communities. IMPORTANCE Understanding the rules governing the composition of the diverse microbial communities that reside in the vertebrate gut environment will enhance our ability to manipulate such communities for therapeutic ends. Synthetic microbial communities, assembled from specific combinations of microbial species in germfree animals, allow investigation of the fundamental question of whether multispecies community composition can be predicted solely based on the combined effects of interactions between pairs of species. If so, such predictability would enable the construction of communities with desired species from the bottom up. If not, the apparent higher-order interactions imply that emergent community-level characteristics are crucial. Our findings using up to five coexisting native bacterial species in larval zebrafish, a model vertebrate, provide experimental evidence for higher-order interactions and, moreover, show that these interactions promote the coexistence of microbial species in the gut.Deepika SundarramanEdouard A. HayDylan M. MartinsDrew S. ShieldsNoah L. PettinariRaghuveer ParthasarathyAmerican Society for Microbiologyarticlegut microbiomemicrobial interactionszebrafishgnotobioticMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	gut microbiome microbial interactions zebrafish gnotobiotic Microbiology QR1-502
spellingShingle	gut microbiome microbial interactions zebrafish gnotobiotic Microbiology QR1-502 Deepika Sundarraman Edouard A. Hay Dylan M. Martins Drew S. Shields Noah L. Pettinari Raghuveer Parthasarathy Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
description	ABSTRACT The microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health, and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial composition remain largely unknown. Further, it is unclear for many multispecies consortia whether their species-level makeup can be predicted based on an understanding of pairwise species interactions or whether higher-order interactions are needed to explain emergent compositions. To address this, we examine commensal intestinal microbes in larval zebrafish, initially raised germfree, to allow the introduction of controlled combinations of bacterial species. Using a dissection and plating assay, we demonstrate the construction of communities of one to five bacterial species and show that the outcomes from the two-species competitions fail to predict species abundances in more complex communities. With multiple species present, interbacterial interactions become weaker, suggesting that higher-order interactions in the vertebrate gut stabilize complex communities. IMPORTANCE Understanding the rules governing the composition of the diverse microbial communities that reside in the vertebrate gut environment will enhance our ability to manipulate such communities for therapeutic ends. Synthetic microbial communities, assembled from specific combinations of microbial species in germfree animals, allow investigation of the fundamental question of whether multispecies community composition can be predicted solely based on the combined effects of interactions between pairs of species. If so, such predictability would enable the construction of communities with desired species from the bottom up. If not, the apparent higher-order interactions imply that emergent community-level characteristics are crucial. Our findings using up to five coexisting native bacterial species in larval zebrafish, a model vertebrate, provide experimental evidence for higher-order interactions and, moreover, show that these interactions promote the coexistence of microbial species in the gut.
format	article
author	Deepika Sundarraman Edouard A. Hay Dylan M. Martins Drew S. Shields Noah L. Pettinari Raghuveer Parthasarathy
author_facet	Deepika Sundarraman Edouard A. Hay Dylan M. Martins Drew S. Shields Noah L. Pettinari Raghuveer Parthasarathy
author_sort	Deepika Sundarraman
title	Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
title_short	Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
title_full	Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
title_fullStr	Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
title_full_unstemmed	Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome
title_sort	higher-order interactions dampen pairwise competition in the zebrafish gut microbiome
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/dc5d529796de45a2bbd3310ea1ec123f
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Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

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