School of Biological Sciences, University of Utah, Salt Lake City, UT 84112;
School of Biological Sciences, University of Utah, Salt Lake City, UT 84112.
Proc Natl Acad Sci U S A. 2021 Nov 23;118(47). doi: 10.1073/pnas.2108787118.
The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus , we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.
微生物组对于宿主的生存和适应至关重要,但我们对于这种共生群落的结构如何形成仍存在认识上的差距。尽管有证据表明,相关宿主通常拥有相似的细菌群落,但尚不清楚这种模式是由于宿主之间的遗传相似性还是由于共同的生态选择压力所致。在这里,我们使用 属的食草啮齿动物,量化了地理、饮食、宿主遗传以及中性过程如何在自然和圈养条件下影响微生物组的结构和稳定性。我们使用细菌和植物代谢组学,首先对来自 25 个种群的动物的饮食和微生物组组成进行了特征描述,这些动物代表了美国西南部 19 个地点的 7 个物种。然后,我们将野生动物带入圈养环境,减少了环境变化的影响。在自然界中,地理、饮食和系统发育共同解释了约 50%的观察到的微生物组变异。饮食和微生物组多样性呈正相关,不同的毒素富集饮食选择了不同的微生物共生体。尽管饮食和地理影响了自然微生物组的结构,但宿主系统发育的影响对于野生和圈养动物都更为强烈。在圈养环境中,肠道微生物组发生了改变;然而,反应是物种特异性的,这再次表明宿主遗传背景是微生物组组成和稳定性的最重要预测因子。在圈养环境中,饮食的影响减弱,而宿主遗传相似性的影响增强。通过在野生和圈养动物研究之间架起一座关键的桥梁,这项工作突出了遗传因素在塑造密切相关宿主的微生物组结构和稳定性方面的程度。