Epidemiology of Highly Pathogenic Organisms, Robert Koch Institute, 13353 Berlin, Germany;
Viral Evolution, Robert Koch Institute, 13353 Berlin, Germany.
Proc Natl Acad Sci U S A. 2021 Apr 13;118(15). doi: 10.1073/pnas.2013535118.
Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health. However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations. We find relatives of the majority of human-associated phages in wild primates. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost codivergence is often detected for individual phages. Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior. Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans. Phage phylogenies reveal replacement of wild great ape-associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity. Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution. Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity.
人类体内栖息着多样的微生物群落，其中大部分是胃肠道内的细菌。这些肠道细菌群落反过来又拥有多样的噬菌体（以下简称噬菌体）群落，这些噬菌体对其结构、功能，最终对人类健康产生重大影响。然而，这些与人类相关的噬菌体群落的进化和生态起源仍知之甚少。为了解决这个问题，我们检测了 23 种野生非人类灵长类动物的粪便噬菌体组，其中包括所有主要灵长类动物辐射的多个代表。我们在野生灵长类动物中发现了与大多数人类相关噬菌体的亲缘关系。灵长类动物具有独特的噬菌体组组成，表现出明显的 phylosymbiotic 信号，并且经常检测到个别噬菌体的噬菌体-超级宿主共进化。在物种内，相邻的社会群体拥有组成和进化上不同的噬菌体组，这些噬菌体组由超级宿主的社会行为结构。圈养非人类灵长类动物的噬菌体组组成介于其野生对应物和人类之间。噬菌体系统发育揭示了在圈养中，野生大猿相关噬菌体被人类相关噬菌体所取代，令人惊讶的是，在圈养中没有野生相关噬菌体持续存在的迹象。总之，我们的研究结果表明，潜在不稳定的灵长类-噬菌体关联在数百万年的进化过程中得以维持。在灵长类动物中，这些phylosymbiotic 和有时共进化的噬菌体群落通过群体成员之间的梳理传播而形成，并在灵长类动物被转移到圈养环境中时发生显著改变。
