Primate phageomes are structured by superhost phylogeny and environment

Abstract

The evolutionary origins of human-associated bacteriophage communities are poorly understood.To address this question, we examined fecal phageomes of 23 wild non-human primate taxa, including multiple representatives of all the major primate radiations, and find relatives of the majority of human-associated phages. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost co-divergence is detected for 44 individual phages. Within species, neighboring social groups harbor evolutionarily and compositionally distinct phageomes, structured by superhost social behavior. However, captive non-human primate phageomes are more similar to humans than their wild counterparts, revealing replacement of wild-associated phages with human-associated ones. Together, our results suggest that potentially labile primate-phage associations persisted across millions of years of evolution, potentially facilitated by transmission between groupmates. One Sentence Summary:Relatives of human-associated phages in wild primates reveal ancient but dynamic superhostphage associations shaped by social transmission. Main Text:Mammals harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. Gut bacterial communities in turn host diverse bacteriophage communities that influence their structure, function, colonization patterns, and ultimately superhost health (the superhost is the host for bacteria that in turn host the bacteriophages; 1).

Unexpected higher convergence of human-great ape enteric viromes in central African forest than in a European zoo: A One Health analysis

“…As with gut bacterial microbiota, phylogeny is a strong driver of species-specific enteric virome 20,22,50 . Our findings corroborate a previous investigation of the evolutionary and ecological origins of gut bacteriophage communities (phageome), demonstrating that the phageome structure and dynamics were influenced by superhost phylogeny and environment 51 .…”

Key features of the genetic architecture and evolution of host-microbe interactions revealed by high-resolution genetic mapping of the mucosa-associated gut microbiome in hybrid mice

“…An intriguing observation made in comparative microbiome research in the last decade is that the pattern of diversification among gut microbiomes appears to mirror host phylogeny (Ochman et al, 2010). This phenomenon, coined "phylosymbiosis" (Brucker and Bordenstein, 2012a;Brucker and Bordenstein, 2012b;Lim and Bordenstein, 2020), is documented in a number of diverse host taxa (Brooks et al, 2016) and also extends to the level of the phageome (Gogarten et al, 2021). Several non-mutually exclusive hypotheses are proposed to explain phylosymbiosis (Moran and Sloan, 2015).…”