Bornbusch Sally L, Greene Lydia K, Rahobilalaina Sylvia, Calkins Samantha, Rothman Ryan S, Clarke Tara A, LaFleur Marni, Drea Christine M
Department of Evolutionary Anthropology, Duke University, Durham, NC, USA.
Duke Lemur Center, Durham, NC, USA.
Anim Microbiome. 2022 Apr 28;4(1):29. doi: 10.1186/s42523-022-00176-x.
Inter-population variation in host-associated microbiota reflects differences in the hosts' environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes-an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia.
The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal 'signal of captivity' that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota.
As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple 'captive vs. wild' dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.
宿主相关微生物群的种群间差异反映了宿主环境的差异，但这种特征描述通常基于比较少数种群的研究。在这些比较中，尚未涵盖任何给定宿主物种所占据的自然栖息地和圈养条件的多样性。此外，肠道微生物群的种内变异通常归因于饮食，也可能源于环境微生物的差异获取——这是一种尚未得到充分研究的机制，通过该机制宿主微生物群直接受到环境微生物的塑造。为了更全面地描述生态适应性强的环尾狐猴（Lemur catta；n = 209）的肠道微生物群，同时研究环境获取的作用，我们对从多达13个地点采集的狐猴肠道和土壤微生物群进行了16S rRNA测序，其中8个地点位于马达加斯加的野外，5个地点位于马达加斯加或美国的圈养环境中。基于匹配的粪便和土壤样本，我们使用微生物源追踪来检查这两种菌群之间的协变关系。
狐猴肠道微生物的多样性在不同地点内部和之间都有显著差异。野生狐猴的微生物多样性并不总是高于圈养狐猴，这表明该指标不一定是宿主栖息地或环境条件的指标。微生物组成的变异既不符合野生同种动物单一的代表性肠道群落，也不符合使圈养动物肠道菌群同质化的普遍“圈养信号”。尽管两大洲的圈养狐猴食用相似的商业饲料，但马达加斯加境内的狐猴肠道微生物群在组成上最为相似，这表明非饮食因素控制着部分变异性。特别是，土壤微生物群落在不同地理位置存在差异，来自不同大陆的少数样本最为独特，并且肠道和土壤微生物群之间存在显著的、特定背景的协变关系。
作为对灵长类微生物群最广泛的单物种研究之一，我们的研究强调肠道菌群对多种环境差异尺度敏感。这一发现需要重新评估简单的“圈养与野生”二分法。除了对动物护理、健康和保护具有重要意义外，我们发现环境获取可能介导宿主相关菌群的各个方面，这进一步扩展了宿主相关微生物和环境微生物在不同微生物景观中相互作用的框架。
