Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome
Abstract Introduction Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and intriguing patterns of site specificity amidst the lack of dispersal limitation. However, the determinants of niche partitioning in this habitat a...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-12-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-020-02195-w |
| _version_ | 1819077591322066944 |
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| author | Alon Shaiber Amy D. Willis Tom O. Delmont Simon Roux Lin-Xing Chen Abigail C. Schmid Mahmoud Yousef Andrea R. Watson Karen Lolans Özcan C. Esen Sonny T. M. Lee Nora Downey Hilary G. Morrison Floyd E. Dewhirst Jessica L. Mark Welch A. Murat Eren |
| author_facet | Alon Shaiber Amy D. Willis Tom O. Delmont Simon Roux Lin-Xing Chen Abigail C. Schmid Mahmoud Yousef Andrea R. Watson Karen Lolans Özcan C. Esen Sonny T. M. Lee Nora Downey Hilary G. Morrison Floyd E. Dewhirst Jessica L. Mark Welch A. Murat Eren |
| author_sort | Alon Shaiber |
| collection | DOAJ |
| description | Abstract Introduction Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and intriguing patterns of site specificity amidst the lack of dispersal limitation. However, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among taxa that belong to recently discovered branches of microbial life. Results Here, we assemble metagenomes from tongue and dental plaque samples from multiple individuals and reconstruct 790 non-redundant genomes, 43 of which resolve to TM7, a member of the Candidate Phyla Radiation, forming six monophyletic clades that distinctly associate with either plaque or tongue. Both pangenomic and phylogenomic analyses group tongue-specific clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 group with environmental TM7 genomes. Besides offering deeper insights into the ecology, evolution, and mobilome of cryptic members of the oral microbiome, our study reveals an intriguing resemblance between dental plaque and non-host environments indicated by the TM7 evolution, suggesting that plaque may have served as a stepping stone for environmental microbes to adapt to host environments for some clades of microbes. Additionally, we report that prophages are widespread among oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment. Conclusions Our data illuminate niche partitioning of enigmatic members of the oral cavity, including TM7, SR1, and GN02, and provide genomes for poorly characterized yet prevalent members of this biome, such as uncultivated Flavobacteriaceae. |
| first_indexed | 2024-12-21T18:59:38Z |
| format | Article |
| id | doaj.art-a6fb499471734e1d8c8eb15a4b66f129 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-12-21T18:59:38Z |
| publishDate | 2020-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-a6fb499471734e1d8c8eb15a4b66f1292022-12-21T18:53:30ZengBMCGenome Biology1474-760X2020-12-0121113510.1186/s13059-020-02195-wFunctional and genetic markers of niche partitioning among enigmatic members of the human oral microbiomeAlon Shaiber0Amy D. Willis1Tom O. Delmont2Simon Roux3Lin-Xing Chen4Abigail C. Schmid5Mahmoud Yousef6Andrea R. Watson7Karen Lolans8Özcan C. Esen9Sonny T. M. Lee10Nora Downey11Hilary G. Morrison12Floyd E. Dewhirst13Jessica L. Mark Welch14A. Murat Eren15Department of Medicine, University of ChicagoDepartment of Biostatistics, University of WashingtonGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayDepartment of Energy Joint Genome InstituteDepartment of Earth and Planetary Sciences, University of CaliforniaComputational and Applied Mathematics, University of ChicagoComputer Science, University of ChicagoDepartment of Medicine, University of ChicagoDepartment of Medicine, University of ChicagoDepartment of Medicine, University of ChicagoDivision of Biology, Kansas State UniversityJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryDepartment of Microbiology, The Forsyth InstituteJosephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological LaboratoryDepartment of Medicine, University of ChicagoAbstract Introduction Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and intriguing patterns of site specificity amidst the lack of dispersal limitation. However, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among taxa that belong to recently discovered branches of microbial life. Results Here, we assemble metagenomes from tongue and dental plaque samples from multiple individuals and reconstruct 790 non-redundant genomes, 43 of which resolve to TM7, a member of the Candidate Phyla Radiation, forming six monophyletic clades that distinctly associate with either plaque or tongue. Both pangenomic and phylogenomic analyses group tongue-specific clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 group with environmental TM7 genomes. Besides offering deeper insights into the ecology, evolution, and mobilome of cryptic members of the oral microbiome, our study reveals an intriguing resemblance between dental plaque and non-host environments indicated by the TM7 evolution, suggesting that plaque may have served as a stepping stone for environmental microbes to adapt to host environments for some clades of microbes. Additionally, we report that prophages are widespread among oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment. Conclusions Our data illuminate niche partitioning of enigmatic members of the oral cavity, including TM7, SR1, and GN02, and provide genomes for poorly characterized yet prevalent members of this biome, such as uncultivated Flavobacteriaceae.https://doi.org/10.1186/s13059-020-02195-wMetagenomicsMetapangenomicsNiche partitioningHuman oral cavityCandidate phyla radiationSaccharibacteria |
| spellingShingle | Alon Shaiber Amy D. Willis Tom O. Delmont Simon Roux Lin-Xing Chen Abigail C. Schmid Mahmoud Yousef Andrea R. Watson Karen Lolans Özcan C. Esen Sonny T. M. Lee Nora Downey Hilary G. Morrison Floyd E. Dewhirst Jessica L. Mark Welch A. Murat Eren Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome Genome Biology Metagenomics Metapangenomics Niche partitioning Human oral cavity Candidate phyla radiation Saccharibacteria |
| title | Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| title_full | Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| title_fullStr | Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| title_full_unstemmed | Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| title_short | Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| title_sort | functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome |
| topic | Metagenomics Metapangenomics Niche partitioning Human oral cavity Candidate phyla radiation Saccharibacteria |
| url | https://doi.org/10.1186/s13059-020-02195-w |
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