The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals

ABSTRACT The human microbiome is affected by multiple factors, including the environment and host genetics. In this study, we analyzed the salivary microbiomes of an extended family of Ashkenazi Jewish individuals living in several cities and investigated associations with both shared household and...

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Autores principales:	Liam Shaw, Andre L. R. Ribeiro, Adam P. Levine, Nikolas Pontikos, Francois Balloux, Anthony W. Segal, Adam P. Roberts, Andrew M. Smith
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	environmental microbiology microbiome oral microbiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c7f5b16c28f749aca4fdc8637d8c3156
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spelling	oai:doaj.org-article:c7f5b16c28f749aca4fdc8637d8c31562021-11-15T15:51:51ZThe Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals10.1128/mBio.01237-172150-7511https://doaj.org/article/c7f5b16c28f749aca4fdc8637d8c31562017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01237-17https://doaj.org/toc/2150-7511ABSTRACT The human microbiome is affected by multiple factors, including the environment and host genetics. In this study, we analyzed the salivary microbiomes 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 effects. While there was weak evidence of geographical structuring at the level of cities, we observed a large and significant effect of shared household on microbiome composition, supporting the role of the 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 salivary 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 the environment rather than host genetics is the dominant factor affecting the composition of the salivary 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 a shared living environment significantly affect microbial community composition. IMPORTANCE Previous research shows that the salivary microbiomes of relatives are more similar than those of nonrelatives, 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 single nucleotide polymorphisms (SNPs) (rather than pedigree measures) and shared environment in the same analysis. We quantify the relative importance of these factors by studying the salivary microbiomes in members of a large extended Ashkenazi Jewish family living in different locations. We find that host genetics plays no significant role and that the dominant factor is the 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 aspects of salivary microbiome composition established during upbringing can persist over a time scale of years.Liam ShawAndre L. R. RibeiroAdam P. LevineNikolas PontikosFrancois BallouxAnthony W. SegalAdam P. RobertsAndrew M. SmithAmerican Society for Microbiologyarticleenvironmental microbiologymicrobiomeoral microbiologyMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	environmental microbiology microbiome oral microbiology Microbiology QR1-502
spellingShingle	environmental microbiology microbiome oral microbiology Microbiology QR1-502 Liam Shaw Andre L. R. Ribeiro Adam P. Levine Nikolas Pontikos Francois Balloux Anthony W. Segal Adam P. Roberts Andrew M. Smith The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
description	ABSTRACT The human microbiome is affected by multiple factors, including the environment and host genetics. In this study, we analyzed the salivary microbiomes 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 effects. While there was weak evidence of geographical structuring at the level of cities, we observed a large and significant effect of shared household on microbiome composition, supporting the role of the 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 salivary 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 the environment rather than host genetics is the dominant factor affecting the composition of the salivary 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 a shared living environment significantly affect microbial community composition. IMPORTANCE Previous research shows that the salivary microbiomes of relatives are more similar than those of nonrelatives, 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 single nucleotide polymorphisms (SNPs) (rather than pedigree measures) and shared environment in the same analysis. We quantify the relative importance of these factors by studying the salivary microbiomes in members of a large extended Ashkenazi Jewish family living in different locations. We find that host genetics plays no significant role and that the dominant factor is the 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 aspects of salivary microbiome composition established during upbringing can persist over a time scale of years.
format	article
author	Liam Shaw Andre L. R. Ribeiro Adam P. Levine Nikolas Pontikos Francois Balloux Anthony W. Segal Adam P. Roberts Andrew M. Smith
author_facet	Liam Shaw Andre L. R. Ribeiro Adam P. Levine Nikolas Pontikos Francois Balloux Anthony W. Segal Adam P. Roberts Andrew M. Smith
author_sort	Liam Shaw
title	The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
title_short	The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
title_full	The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
title_fullStr	The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
title_full_unstemmed	The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals
title_sort	human salivary microbiome is shaped by shared environment rather than genetics: evidence from a large family of closely related individuals
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/c7f5b16c28f749aca4fdc8637d8c3156
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The Human Salivary Microbiome Is Shaped by Shared Environment Rather than Genetics: Evidence from a Large Family of Closely Related Individuals

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