Supragingival plaque microbiome ecology and functional potential in the context of health and disease

Josh L. Espinoza; Derek M. Harkins; Manolito Torralba; Andres Gomez; Sarah K. Highlander; Marcus B. Jones; Pamela Leong; Richard Saffery; Michelle Bockmann; Claire Kuelbs; Jason M. Inman; Toby Hughes; Jeffrey M. Craig; Karen E. Nelson; Chris L. Dupont

doi:10.1128/mBio.01631-18

Supragingival plaque microbiome ecology and functional potential in the context of health and disease

Josh L. Espinoza, Derek M. Harkins, Manolito Torralba, Andres Gomez, Sarah K. Highlander, Marcus B. Jones, Pamela Leong, Richard Saffery, Michelle Bockmann, Claire Kuelbs, Jason M. Inman, Toby Hughes, Jeffrey M. Craig, Karen E. Nelson, Chris L. Dupont

Animal Science

Research output: Contribution to journal › Article › peer-review

16 Scopus citations

Abstract

To address the question of how microbial diversity and function in the oral cavities of children relates to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. Caries phenotypes contained statistically significant enrichments in specific genome abundances and distinct community composition profiles, including strain-level changes. Metabolic pathways that are statistically associated with caries include several sugar-associated phosphotransferase systems, antimicrobial resistance, and metal transport. Numerous closely related previously uncharacterized microbes had substantial variation in central metabolism, including the loss of biosynthetic pathways resulting in auxotrophy, changing the ecological role. We also describe the first complete Gracilibacteria genomes from the human microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries. IMPORTANCE Oral health has substantial economic importance, with over $100 billion spent on dental care in the United States annually. The microbiome plays a critical role in oral health, yet remains poorly classified. To address the question of how microbial diversity and function in the oral cavities of children relate to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. This unveiled several new previously uncharacterized but ubiquitous microbial lineages in the oral microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries.

Original language	English (US)
Article number	e01631-18
Journal	mBio
Volume	9
Issue number	6
DOIs	https://doi.org/10.1128/mBio.01631-18
State	Published - Nov 1 2018

Bibliographical note

Funding Information:
The research in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under award number R01DE019665. PETS was supported by grants from the Australian National Health and Medical Research Council (grant numbers 437015 and 607358 to J.M.C. and R.S.), the Bonnie Babes Foundation (grant number BBF20704 to J.M.C.), the Financial Markets Foundation for Children (grant no. 032-2007 to J.M.C.), and the Victorian Government’s Operational Infrastructure Support Program. CBRG was supported by grants from the Australian National Health and Medical Research Council (grant numbers 349448 and 1006294 to T.H.) and the Financial Markets Foundation for Children (grant no. 223-2009 to T.H.).

Funding Information:
We thank all twins and their families; Grant Townsend and Nicky Kilpatrick for their dental expertise; Tina Vaiano, Jane Loke, Anna Czajko, Blessy Manil, Chrissie Robinson, Mihiri Silva, and Supriya Raj for their expertise and assistance with collection of data and samples; and Anna Edlund for constructive comments on an early draft of the manuscript. The research in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under award number R01DE019665. PETS was supported by grants from the Australian National Health and Medical Research Council (grant numbers 437015 and 607358 to J.M.C. and R.S.), the Bonnie Babes Foundation (grant number BBF20704‏ to ‏J.M.‏C.‏), the Financial Markets Foundation for Children (grant no. 032-2007 to J.M.C.), and the Victorian Government’s Operational Infrastructure Support Program. CBRG was supported by grants from the Australian National Health and Medical Research Council (grant numbers 349448 and 1006294 to T.H.) and the Financial Markets Foundation for Children (grant no. 223-2009 to T.H.). J.L.E. conducted the majority of the data analysis with contributions from C.L.D., J.M.I., and D.M.H. M.T. and C.K. conducted sample extractions and oversaw sequencing. A.G.‏, S.‏K.H.‏, and M.B.J.‏ were involved in pr‏oj‏ect coordinati‏on‏ during th‏e sample gat‏hering phase. P.L., R.S., M.B., T.H., and J.M.C. oversaw clinical sampling. K.E.N. attained funding and guided the research. C.L.D. ‏dire‏cted‏ t‏he data analysis and interpretation. C.L.D. and J.L.E. wrote the paper with contributions from all authors. The authors declare no competing interests.

Publisher Copyright:
© 2018 Espinoza et al.

Keywords

Metabolism
Metagenomics
Microbial ecology
Oral microbiology
Streptococcus

UN SDGs

This output contributes to the following Sustainable Development Goal(s)

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Espinoza, J. L., Harkins, D. M., Torralba, M., Gomez, A., Highlander, S. K., Jones, M. B., Leong, P., Saffery, R., Bockmann, M., Kuelbs, C., Inman, J. M., Hughes, T., Craig, J. M., Nelson, K. E., & Dupont, C. L. (2018). Supragingival plaque microbiome ecology and functional potential in the context of health and disease. mBio, 9(6), [e01631-18]. https://doi.org/10.1128/mBio.01631-18

Supragingival plaque microbiome ecology and functional potential in the context of health and disease. / Espinoza, Josh L.; Harkins, Derek M.; Torralba, Manolito; Gomez, Andres; Highlander, Sarah K.; Jones, Marcus B.; Leong, Pamela; Saffery, Richard; Bockmann, Michelle; Kuelbs, Claire; Inman, Jason M.; Hughes, Toby; Craig, Jeffrey M.; Nelson, Karen E.; Dupont, Chris L.

In: mBio, Vol. 9, No. 6, e01631-18, 01.11.2018.

Research output: Contribution to journal › Article › peer-review

Espinoza, Josh L. ; Harkins, Derek M. ; Torralba, Manolito ; Gomez, Andres ; Highlander, Sarah K. ; Jones, Marcus B. ; Leong, Pamela ; Saffery, Richard ; Bockmann, Michelle ; Kuelbs, Claire ; Inman, Jason M. ; Hughes, Toby ; Craig, Jeffrey M. ; Nelson, Karen E. ; Dupont, Chris L. / Supragingival plaque microbiome ecology and functional potential in the context of health and disease. In: mBio. 2018 ; Vol. 9, No. 6.

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abstract = "To address the question of how microbial diversity and function in the oral cavities of children relates to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. Caries phenotypes contained statistically significant enrichments in specific genome abundances and distinct community composition profiles, including strain-level changes. Metabolic pathways that are statistically associated with caries include several sugar-associated phosphotransferase systems, antimicrobial resistance, and metal transport. Numerous closely related previously uncharacterized microbes had substantial variation in central metabolism, including the loss of biosynthetic pathways resulting in auxotrophy, changing the ecological role. We also describe the first complete Gracilibacteria genomes from the human microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries. IMPORTANCE Oral health has substantial economic importance, with over $100 billion spent on dental care in the United States annually. The microbiome plays a critical role in oral health, yet remains poorly classified. To address the question of how microbial diversity and function in the oral cavities of children relate to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. This unveiled several new previously uncharacterized but ubiquitous microbial lineages in the oral microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries.",

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note = "Funding Information: The research in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under award number R01DE019665. PETS was supported by grants from the Australian National Health and Medical Research Council (grant numbers 437015 and 607358 to J.M.C. and R.S.), the Bonnie Babes Foundation (grant number BBF20704 to J.M.C.), the Financial Markets Foundation for Children (grant no. 032-2007 to J.M.C.), and the Victorian Government{\textquoteright}s Operational Infrastructure Support Program. CBRG was supported by grants from the Australian National Health and Medical Research Council (grant numbers 349448 and 1006294 to T.H.) and the Financial Markets Foundation for Children (grant no. 223-2009 to T.H.). Funding Information: We thank all twins and their families; Grant Townsend and Nicky Kilpatrick for their dental expertise; Tina Vaiano, Jane Loke, Anna Czajko, Blessy Manil, Chrissie Robinson, Mihiri Silva, and Supriya Raj for their expertise and assistance with collection of data and samples; and Anna Edlund for constructive comments on an early draft of the manuscript. The research in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under award number R01DE019665. PETS was supported by grants from the Australian National Health and Medical Research Council (grant numbers 437015 and 607358 to J.M.C. and R.S.), the Bonnie Babes Foundation (grant number BBF20704‏ to ‏J.M.‏C.‏), the Financial Markets Foundation for Children (grant no. 032-2007 to J.M.C.), and the Victorian Government{\textquoteright}s Operational Infrastructure Support Program. CBRG was supported by grants from the Australian National Health and Medical Research Council (grant numbers 349448 and 1006294 to T.H.) and the Financial Markets Foundation for Children (grant no. 223-2009 to T.H.). J.L.E. conducted the majority of the data analysis with contributions from C.L.D., J.M.I., and D.M.H. M.T. and C.K. conducted sample extractions and oversaw sequencing. A.G.‏, S.‏K.H.‏, and M.B.J.‏ were involved in pr‏oj‏ect coordinati‏on‏ during th‏e sample gat‏hering phase. P.L., R.S., M.B., T.H., and J.M.C. oversaw clinical sampling. K.E.N. attained funding and guided the research. C.L.D. ‏dire‏cted‏ t‏he data analysis and interpretation. C.L.D. and J.L.E. wrote the paper with contributions from all authors. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2018 Espinoza et al.",

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AU - Harkins, Derek M.

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AU - Gomez, Andres

AU - Highlander, Sarah K.

AU - Jones, Marcus B.

AU - Leong, Pamela

AU - Saffery, Richard

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N2 - To address the question of how microbial diversity and function in the oral cavities of children relates to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. Caries phenotypes contained statistically significant enrichments in specific genome abundances and distinct community composition profiles, including strain-level changes. Metabolic pathways that are statistically associated with caries include several sugar-associated phosphotransferase systems, antimicrobial resistance, and metal transport. Numerous closely related previously uncharacterized microbes had substantial variation in central metabolism, including the loss of biosynthetic pathways resulting in auxotrophy, changing the ecological role. We also describe the first complete Gracilibacteria genomes from the human microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries. IMPORTANCE Oral health has substantial economic importance, with over $100 billion spent on dental care in the United States annually. The microbiome plays a critical role in oral health, yet remains poorly classified. To address the question of how microbial diversity and function in the oral cavities of children relate to caries diagnosis, we surveyed the supragingival plaque biofilm microbiome in 44 juvenile twin pairs. Using shotgun sequencing, we constructed a genome encyclopedia describing the core supragingival plaque microbiome. This unveiled several new previously uncharacterized but ubiquitous microbial lineages in the oral microbiome. Caries is a microbial community metabolic disorder that cannot be described by a single etiology, and our results provide the information needed for next-generation diagnostic tools and therapeutics for caries.

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KW - Streptococcus

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Supragingival plaque microbiome ecology and functional potential in the context of health and disease

Abstract

Bibliographical note

Keywords

UN SDGs

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