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

Liam Shaw,Adam P Levine,Nikolas Pontikos,Andre L R Ribeiro,Francois Balloux,Adam P Roberts,Andrew M Smith,Anthony W Segal,Claire M Fraser

doi:10.1128/mbio.01237-17

Abstract

ABSTRACTThe 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.

Highlights

The human microbiome is affected by multiple factors, including the environment and host genetics
We found a weak correlation between host kinship and salivary microbiome dissimilarity before taking shared household into account and an apparent small but significant effect of genetics when using kinships based on the family pedigree as proxies for genetic similarity
When using kinship estimates based on genome-wide single nucleotide polymorphisms (SNPs) between individuals and simultaneously controlling for shared household with a permutational analysis of variance, we find no support for any clear effect of human genetics, suggesting that shared environment has a much larger effect than genetics and is the dominant factor affecting the salivary microbiome

Summary

Introduction

The human microbiome is affected by multiple factors, including the environment and host genetics. 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 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. The effect of cohabitation with direct and frequent contact is greatest when considering the skin microbiome, with a less-evident effect on the gut and salivary microbiomes [11]

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Discussion

Conclusion