Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria

ABSTRACT Candidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earth’s ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions among these habitats remain unclear. Here, we expand the ge...

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Autores principales:	Alexander L. Jaffe, Alex D. Thomas, Christine He, Ray Keren, Luis E. Valentin-Alvarado, Patrick Munk, Keith Bouma-Gregson, Ibrahim F. Farag, Yuki Amano, Rohan Sachdeva, Patrick T. West, Jillian F. Banfield
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	CPR bacteria animal microbiome bacterial evolution comparative genomics habitat transition Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cafaa700979043c3bf6649332329a31c
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spelling	oai:doaj.org-article:cafaa700979043c3bf6649332329a31c2021-11-10T18:37:50ZPatterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria10.1128/mBio.00521-212150-7511https://doaj.org/article/cafaa700979043c3bf6649332329a31c2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00521-21https://doaj.org/toc/2150-7511ABSTRACT Candidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earth’s ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions among these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that animal-associated Saccharibacteria have smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa and were reinforced by acquisition and loss of some capacities. IMPORTANCE Studying the genetic differences between related microorganisms from different environment types can indicate factors associated with their movement among habitats. This is particularly interesting for bacteria from the Candidate Phyla Radiation because their minimal metabolic capabilities require associations with microbial hosts. We found that shifts of Absconditabacteria, Gracilibacteria, and Saccharibacteria between environmental ecosystems and mammalian mouths/guts probably did not involve major episodes of gene gain and loss; rather, gradual genomic change likely followed habitat migration. The results inform our understanding of how little-known microorganisms establish in the human microbiota where they may ultimately impact health.Alexander L. JaffeAlex D. ThomasChristine HeRay KerenLuis E. Valentin-AlvaradoPatrick MunkKeith Bouma-GregsonIbrahim F. FaragYuki AmanoRohan SachdevaPatrick T. WestJillian F. BanfieldAmerican Society for MicrobiologyarticleCPR bacteriaanimal microbiomebacterial evolutioncomparative genomicshabitat transitionMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	CPR bacteria animal microbiome bacterial evolution comparative genomics habitat transition Microbiology QR1-502
spellingShingle	CPR bacteria animal microbiome bacterial evolution comparative genomics habitat transition Microbiology QR1-502 Alexander L. Jaffe Alex D. Thomas Christine He Ray Keren Luis E. Valentin-Alvarado Patrick Munk Keith Bouma-Gregson Ibrahim F. Farag Yuki Amano Rohan Sachdeva Patrick T. West Jillian F. Banfield Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
description	ABSTRACT Candidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earth’s ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions among these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that animal-associated Saccharibacteria have smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa and were reinforced by acquisition and loss of some capacities. IMPORTANCE Studying the genetic differences between related microorganisms from different environment types can indicate factors associated with their movement among habitats. This is particularly interesting for bacteria from the Candidate Phyla Radiation because their minimal metabolic capabilities require associations with microbial hosts. We found that shifts of Absconditabacteria, Gracilibacteria, and Saccharibacteria between environmental ecosystems and mammalian mouths/guts probably did not involve major episodes of gene gain and loss; rather, gradual genomic change likely followed habitat migration. The results inform our understanding of how little-known microorganisms establish in the human microbiota where they may ultimately impact health.
format	article
author	Alexander L. Jaffe Alex D. Thomas Christine He Ray Keren Luis E. Valentin-Alvarado Patrick Munk Keith Bouma-Gregson Ibrahim F. Farag Yuki Amano Rohan Sachdeva Patrick T. West Jillian F. Banfield
author_facet	Alexander L. Jaffe Alex D. Thomas Christine He Ray Keren Luis E. Valentin-Alvarado Patrick Munk Keith Bouma-Gregson Ibrahim F. Farag Yuki Amano Rohan Sachdeva Patrick T. West Jillian F. Banfield
author_sort	Alexander L. Jaffe
title	Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
title_short	Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
title_full	Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
title_fullStr	Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
title_full_unstemmed	Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria
title_sort	patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in candidate phyla radiation bacteria
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/cafaa700979043c3bf6649332329a31c
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Patterns of Gene Content and Co-occurrence Constrain the Evolutionary Path toward Animal Association in Candidate Phyla Radiation Bacteria

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