Acquisition of oral microbiota is driven by environment, not host genetics

Abstract

Background The oral microbiota is acquired very early, but the factors shaping its acquisition are not well understood. Previous studies comparing monozygotic (MZ) and dizygotic (DZ) twins have suggested that host genetics plays a role. However, all twins share an equal portion of their parent’s genome, so this model is not informative for studying parent-to-child transmission. We used a novel study design that allowed us to directly examine the genetics of transmission by comparing the oral microbiota of biological versus adoptive mother-child dyads. Results No difference was observed in how closely oral bacterial community profiles matched for adoptive versus biological mother-child pairs, indicating little if any effect of host genetics on the fidelity of transmission. Both adopted and biologic children more closely resembled their own mother as compared to unrelated women, supporting the role of contact and environment. Mother-child strain similarity increased with the age of the child, ruling out early effects of host genetic influence that are lost over time. No effect on the fidelity of mother-child strain sharing from vaginal birth or breast feeding was seen. Analysis of extended families showed that fathers and mothers were equally similar to their children, and that cohabitating couples showed even greater strain similarity than mother-child pairs. These findings support the role of contact and shared environment, and age, but not genetics, as determinants of microbial transmission, and were consistent at both species and strain level resolutions, and across multiple oral habitats. In addition, analysis of individual species all showed similar results. Conclusions The host is clearly active in shaping the composition of the oral microbiome, since only a few of the many bacterial species in the larger environment are capable of colonizing the human oral cavity. Our findings suggest that these host mechanisms are universally shared among humans, since no effect of genetic relatedness on fidelity of microbial transmission could be detected. Instead our findings point towards contact and shared environment being the driving factors of microbial transmission, with a unique combination of these factors ultimately shaping the highly personalized human oral microbiome.

Early-Life Adversity Leaves Its Imprint on the Oral Microbiome for More Than 20 Years and Is Associated with Long-Term Immune Changes

“…Furthermore, genetically unrelated people with a shared environment show similar environment-related effects on microbiome composition in the mouth as well as other communities [ 43 , 47 , 61 ]. Cohabitation appears to have a greater impact on the skin microbiome rather than gut and oral communities, persisting after the cohabitation is terminated [ 43 , 58 , 60 , 63 ], an effect that is thought to persist for the long term despite leaving or changing household [ 41 , 48 , 49 ].…”

“…Many of these are energy sources for the OM, and salivary glycoproteins are the principal nutrient source. These substrates are crucial for the development of multispecies communities and their preservation [ 41 , 46 , 48 ], and enhance the resistance of the community to environmental stressors [ 41 , 49 , 50 ]. The long-term stability of the OM leads to the hypothesis that, once established in early life, it remains stable, robust, and resilient, retaining an imprint of the early environment [ 42 , 43 ].…”

Oral Microbiota: A Major Player in the Diagnosis of Systemic Diseases

“…Even if the maternal microbiota already plays an important role in the neurodevelopment of the fetus before birth [12,13], the acquisition of the microbiota begins in the first minutes of life through direct contact with the maternal microbiota (skin, vagina, and mouth) [14]. The child's environment is also essential to the construction of its microbiota which is not solely acquired through heredity [4].…”

“…Finally, concerning the transmission of the maternal microbiome to the child, recent research on families with adopted and biological children shows that the composition of the microbiome seems to be shaped more by the host and contact with the local environment than by genetics and direct transfer of this microbiome through pregnancy outcomes and especially delivery modes (C-section or vaginal delivery) [4]. Babies fed only on breast milk have a lower diversity with a decreased relative abundance of Veillonella, Prevotella, Granulicatella, and Porphyromonas than those fed only on formula, but these differences do not persist over time.…”

“…The oral cavity is host to a complex microbial group, the oral microbiota, composed mainly of bacteria but also includes viruses, protozoans, fungi, archaea, phages, and ultrasmall bacteria belonging to the candidate phyla radiation group [1][2][3]. Oral microbiota, developed from the first minutes of a child's life, is composed of more than 500 different bacterial species [4,5]. Its exact composition varies greatly from one individual to another as it depends on several factors, such as age, diet, and lifestyle habits (such as smoking and physical activity) [6].…”