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 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.

Human oral microbiome characterization and its association with environmental microbiome revealed by the Earth Microbiome Project

“…The differences of microbiomes for the same individual at different time points are significantly lower in the oral cavity than in the gut, skin and other body parts [18]. The effects of the early living environment on shaping oral microbes are much more than genetic factors [19]. In addition, lifestyle habits, social factors, and oral pH value also affect the composition of the oral microbiome [20].…”

Acquisition of Oral Microbiota is Driven by Environment, Not Host Genetics

“…In one of three published oral microbiome twin studies 19,20,22 , MZ twin pairs were found to be no more similar than DZ twin pairs, and they became less similar when they no longer cohabited 22 . Kissing couples were observed to share highly similar tongue dorsum microbial communities 23 , and shared household was more important than genetic relationship in a dataset from an extended family 24 . Another study found that household members, particularly couples, shared more of their microbiota than individuals from different households 25 .…”

Portable sequencing, genomic data, and scale in global emerging infectious disease surveillance

“…The microbiome is also personal – gut microbiome samples can be used to uniquely identify individuals from groups of hundreds of others (Franzosa et al., ) – but generally this identifiability decreases with time because the human microbiome is a changing ecosystem that varies with external factors. For example, individuals who live together share more similar microbiomes (Shaw et al., ; Song et al., ) and events like moving abroad or diarrheal illness alter the microbiome (David et al., ). The microbiome therefore contains implicit information about not only individuals’ lifestyles (e.g., their diet and drug intake) but, crucially, social relationships between individuals (e.g., shared households and interaction patterns) (Rothschild et al., ).…”