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The human oral microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely-related individuals

Liam Shaw, Andre L. R. Ribeiro, Adam P. Levine, Nikolas Pontikos, Francois Balloux, Anthony W. Segal, Adam P. Roberts, Andrew M. Smith
doi: https://doi.org/10.1101/131086
Liam Shaw
1UCL Genetics Institute, UCL, London, UK
2Centre for Mathematics and Physics in the Life Sciences and Experimental Biology (CoMPLEX), UCL, London, UK
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Andre L. R. Ribeiro
3UCL Eastman Dental Institute, UCL, London, UK
4School of Dentistry, University Center of Pará – CESUPA, Belém, Brazil
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Adam P. Levine
5Division of Medicine, UCL, London, UK
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Nikolas Pontikos
1UCL Genetics Institute, UCL, London, UK
6Institute of Ophthalmology, UCL, London, UK
7Moorfields Eye Hospital, London, UK
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Francois Balloux
1UCL Genetics Institute, UCL, London, UK
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Anthony W. Segal
5Division of Medicine, UCL, London, UK
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Adam P. Roberts
3UCL Eastman Dental Institute, UCL, London, UK
8Liverpool School of Tropical Medicine, Liverpool, UK
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Andrew M. Smith
3UCL Eastman Dental Institute, UCL, London, UK
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Abstract

The human microbiome is affected by multiple factors, including the environment and host genetics. In this study, we analyzed the oral microbiome of an extended family of Ashkenazi Jewish individuals living in several cities and investigated associations with both shared household and host genetic similarities. We found that environmental effects dominated over genetic ones. While there was weak evidence of geographic structuring at the level of cities, we observed a large and significant effect of shared household on microbiome composition, supporting the role of immediate shared environment in dictating the presence or absence of taxa. This effect was also seen when including adults who had grown up in the same household but moved out prior to the time of sampling, suggesting that the establishment of the oral microbiome earlier in life may affect its long-term composition. We found weak associations between host genetic relatedness and microbiome dissimilarity when using family pedigrees as proxies for genetic similarity. However this association disappeared when using more accurate measures of kinship based on genome-wide genetic markers, indicating that environment rather than host genetics is the dominant factor affecting the composition of the oral microbiome in closely-related individuals. Our results support the concept that there is a consistent core microbiome conserved across global scales, but that small-scale effects due to shared living environment significantly affect microbial community composition.

IMPORTANCE Previous research shows that relatives have a more similar oral microbiome composition than non-relatives, but it remains difficult to distinguish the effects of relatedness and shared household environment. Furthermore, pedigree measures may not accurately measure host genetic similarity. In this study, we include genetic relatedness based on genome-wide SNPs (rather than pedigree measures) and shared environment in the same analysis. We quantify the relative importance of these factors by studying the oral microbiome in members of a large extended Ashkenazi Jewish family who share a similar diet and lifestyle despite living in different locations. We find that host genetics plays no significant role and that the dominant factor is shared environment at the household level. We also find that this effect appears to persist in individuals who have moved out of the parental household, suggesting that the oral microbiome established earlier in life persists long-term.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted April 26, 2017.
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The human oral microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely-related individuals
Liam Shaw, Andre L. R. Ribeiro, Adam P. Levine, Nikolas Pontikos, Francois Balloux, Anthony W. Segal, Adam P. Roberts, Andrew M. Smith
bioRxiv 131086; doi: https://doi.org/10.1101/131086
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The human oral microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely-related individuals
Liam Shaw, Andre L. R. Ribeiro, Adam P. Levine, Nikolas Pontikos, Francois Balloux, Anthony W. Segal, Adam P. Roberts, Andrew M. Smith
bioRxiv 131086; doi: https://doi.org/10.1101/131086

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