From wolves to humans: oral microbiome resistance to transfer across mammalian hosts
ABSTRACT The mammalian mouth is colonized by complex microbial communities, adapted to specific niches, and in homeostasis with the host. Individual microbes interact metabolically and rely primarily on nutrients provided by the host, with which they have potentially co-evolved along the mammalian l...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2024-03-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.03342-23 |
| _version_ | 1827150298465959936 |
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| author | Nicholas A. Podar Alyssa A. Carrell Kira A. Cassidy Dawn M. Klingeman Zamin Yang Erin A. Stahler Douglas W. Smith Daniel R. Stahler Mircea Podar |
| author_facet | Nicholas A. Podar Alyssa A. Carrell Kira A. Cassidy Dawn M. Klingeman Zamin Yang Erin A. Stahler Douglas W. Smith Daniel R. Stahler Mircea Podar |
| author_sort | Nicholas A. Podar |
| collection | DOAJ |
| description | ABSTRACT The mammalian mouth is colonized by complex microbial communities, adapted to specific niches, and in homeostasis with the host. Individual microbes interact metabolically and rely primarily on nutrients provided by the host, with which they have potentially co-evolved along the mammalian lineages. The oral environment is similar across mammals, but the diversity, specificity, and evolution of community structure in related or interacting mammals are little understood. Here, we compared the oral microbiomes of dogs with those of wild wolves and humans. In dogs, we found an increased microbial diversity relative to wolves, possibly related to the transition to omnivorous nutrition following domestication. This includes a larger diversity of Patescibacteria than previously reported in any other oral microbiota. The oral microbes are most distinct at bacterial species or strain levels, with few if any shared between humans and canids, while the close evolutionary relationship between wolves and dogs is reflected by numerous shared taxa. More taxa are shared at higher taxonomic levels including with humans, supporting their more ancestral common mammalian colonization followed by diversification. Phylogenies of selected oral bacterial lineages do not support stable human-dog microbial transfers but suggest diversification along mammalian lineages (apes and canids). Therefore, despite millennia of cohabitation and close interaction, the host and its native community controls and limits the assimilation of new microbes, even if closely related. Higher resolution metagenomic and microbial physiological studies, covering a larger mammalian diversity, should help understand how oral communities assemble, adapt, and interact with their hosts.IMPORTANCENumerous types of microbes colonize the mouth after birth and play important roles in maintaining oral health. When the microbiota-host homeostasis is perturbed, proliferation of some bacteria leads to diseases such as caries and periodontitis. Unlike the gut microbiome, the diversity of oral microbes across the mammalian evolutionary space is not understood. Our study compared the oral microbiomes of wild wolves, dogs, and apes (humans, chimpanzees, and bonobos), with the aim of identifying if microbes have been potentially exchanged between humans and dogs as a result of domestication and cohabitation. We found little if any evidence for such exchanges. The significance of our research is in finding that the oral microbiota and/or the host limit the acquisition of exogenous microbes, which is important in the context of natural exclusion of potential novel pathogens. We provide a framework for expanded higher-resolution studies across domestic and wild animals to understand resistance/resilience. |
| first_indexed | 2024-04-25T00:10:01Z |
| format | Article |
| id | doaj.art-493cbe0ea9464554b4dfa22b18997657 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2025-03-20T21:31:51Z |
| publishDate | 2024-03-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-493cbe0ea9464554b4dfa22b189976572024-08-11T18:12:03ZengAmerican Society for MicrobiologymBio2150-75112024-03-0115310.1128/mbio.03342-23From wolves to humans: oral microbiome resistance to transfer across mammalian hostsNicholas A. Podar0Alyssa A. Carrell1Kira A. Cassidy2Dawn M. Klingeman3Zamin Yang4Erin A. Stahler5Douglas W. Smith6Daniel R. Stahler7Mircea Podar8School of Engineering, Vanderbilt University, Nashville, Tennessee, USABiosciences Department, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USAYellowstone Center for Resources, National Park Service, Yellowstone National Park, Wyoming, USABiosciences Department, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Department, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USAYellowstone Center for Resources, National Park Service, Yellowstone National Park, Wyoming, USAYellowstone Center for Resources, National Park Service, Yellowstone National Park, Wyoming, USAYellowstone Center for Resources, National Park Service, Yellowstone National Park, Wyoming, USABiosciences Department, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USAABSTRACT The mammalian mouth is colonized by complex microbial communities, adapted to specific niches, and in homeostasis with the host. Individual microbes interact metabolically and rely primarily on nutrients provided by the host, with which they have potentially co-evolved along the mammalian lineages. The oral environment is similar across mammals, but the diversity, specificity, and evolution of community structure in related or interacting mammals are little understood. Here, we compared the oral microbiomes of dogs with those of wild wolves and humans. In dogs, we found an increased microbial diversity relative to wolves, possibly related to the transition to omnivorous nutrition following domestication. This includes a larger diversity of Patescibacteria than previously reported in any other oral microbiota. The oral microbes are most distinct at bacterial species or strain levels, with few if any shared between humans and canids, while the close evolutionary relationship between wolves and dogs is reflected by numerous shared taxa. More taxa are shared at higher taxonomic levels including with humans, supporting their more ancestral common mammalian colonization followed by diversification. Phylogenies of selected oral bacterial lineages do not support stable human-dog microbial transfers but suggest diversification along mammalian lineages (apes and canids). Therefore, despite millennia of cohabitation and close interaction, the host and its native community controls and limits the assimilation of new microbes, even if closely related. Higher resolution metagenomic and microbial physiological studies, covering a larger mammalian diversity, should help understand how oral communities assemble, adapt, and interact with their hosts.IMPORTANCENumerous types of microbes colonize the mouth after birth and play important roles in maintaining oral health. When the microbiota-host homeostasis is perturbed, proliferation of some bacteria leads to diseases such as caries and periodontitis. Unlike the gut microbiome, the diversity of oral microbes across the mammalian evolutionary space is not understood. Our study compared the oral microbiomes of wild wolves, dogs, and apes (humans, chimpanzees, and bonobos), with the aim of identifying if microbes have been potentially exchanged between humans and dogs as a result of domestication and cohabitation. We found little if any evidence for such exchanges. The significance of our research is in finding that the oral microbiota and/or the host limit the acquisition of exogenous microbes, which is important in the context of natural exclusion of potential novel pathogens. We provide a framework for expanded higher-resolution studies across domestic and wild animals to understand resistance/resilience.https://journals.asm.org/doi/10.1128/mbio.03342-23oral microbiomemicrobiome evolutionnonhuman microbiotahost-pathogen interactionshost adaptation |
| spellingShingle | Nicholas A. Podar Alyssa A. Carrell Kira A. Cassidy Dawn M. Klingeman Zamin Yang Erin A. Stahler Douglas W. Smith Daniel R. Stahler Mircea Podar From wolves to humans: oral microbiome resistance to transfer across mammalian hosts mBio oral microbiome microbiome evolution nonhuman microbiota host-pathogen interactions host adaptation |
| title | From wolves to humans: oral microbiome resistance to transfer across mammalian hosts |
| title_full | From wolves to humans: oral microbiome resistance to transfer across mammalian hosts |
| title_fullStr | From wolves to humans: oral microbiome resistance to transfer across mammalian hosts |
| title_full_unstemmed | From wolves to humans: oral microbiome resistance to transfer across mammalian hosts |
| title_short | From wolves to humans: oral microbiome resistance to transfer across mammalian hosts |
| title_sort | from wolves to humans oral microbiome resistance to transfer across mammalian hosts |
| topic | oral microbiome microbiome evolution nonhuman microbiota host-pathogen interactions host adaptation |
| url | https://journals.asm.org/doi/10.1128/mbio.03342-23 |
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