Institute for Conservation Research, San Diego Zoo Global, Escondido, California, USA
Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, Mississippi, USA.
mBio. 2019 Apr 9;10(2):e00311-19. doi: 10.1128/mBio.00311-19.
With recent poaching of southern white rhinoceros (SWR []) reaching record levels, the need for a robust assurance population is urgent. However, the global captive SWR population is not currently self-sustaining due to the reproductive failure of captive-born females. Dietary phytoestrogens have been proposed to play a role in this phenomenon, and recent work has demonstrated a negative relationship between diet estrogenicity and fertility of captive-born female SWR. To further examine this relationship, we compared gut microbial communities, fecal phytoestrogens, and fertility of SWR to those of another rhinoceros species-the greater one-horned rhinoceros (GOHR []), which consumes a similar diet but exhibits high levels of fertility in captivity. Using 16S rRNA amplicon sequencing and mass spectrometry, we identified a species-specific fecal microbiota and three dominant fecal phytoestrogen profiles. These profiles exhibited various levels of estrogenicity when tested in an estrogen receptor activation assay for both rhinoceros species, with profiles dominated by the microbial metabolite equol stimulating the highest levels of receptor activation. Finally, we found that SWR fertility varies significantly not only with respect to phytoestrogen profile, but also with respect to the abundance of several bacterial taxa and microbially derived phytoestrogen metabolites. Taken together, these data suggest that in addition to species differences in estrogen receptor sensitivity to phytoestrogens, reproductive outcomes may be driven by the gut microbiota's transformation of dietary phytoestrogens in captive SWR females. Southern white rhinoceros (SWR) poaching has reached record levels, and captive infertility has rendered SWR assurance populations no longer self-sustaining. Previous work has identified dietary phytoestrogens as a likely cause of this problem. Here, we investigate the role of gut microbiota in this phenomenon by comparing two rhinoceros species to provide the first characterizations of gut microbiomes for any rhinoceros species. To our knowledge, our approach, combining parallel sequencing, mass spectrometry, and estrogen receptor activation assays, provides insight into the relationship between microbially mediated phytoestrogen metabolism and fertility that is novel for any vertebrate species. With this information, we plan to direct future work aimed at developing strategies to improve captive reproduction in the hope of alleviating their threat of extinction.
随着最近南部白犀牛（SWR）的偷猎活动达到创纪录水平，对一个强大的保证种群的需求迫在眉睫。然而，由于圈养出生的雌性繁殖失败，全球圈养的 SWR 种群目前无法自我维持。饮食中的植物雌激素被认为在这一现象中起作用，最近的研究表明，饮食雌激素与圈养出生的雌性 SWR 的生育能力呈负相关。为了进一步研究这种关系，我们比较了 SWR 的肠道微生物群落、粪便植物雌激素和生育能力与另一种犀牛物种——印度独角犀（GOHR）的肠道微生物群落、粪便植物雌激素和生育能力，GOHR 消耗相似的饮食，但在圈养中表现出很高的生育能力。使用 16S rRNA 扩增子测序和质谱分析，我们鉴定了一种特定于物种的粪便微生物群和三种主要的粪便植物雌激素谱。当在两种犀牛的雌激素受体激活测定中测试这些谱时，它们表现出不同程度的雌激素活性，其中由微生物代谢物 equol 主导的谱刺激受体激活的水平最高。最后，我们发现 SWR 的生育能力不仅与植物雌激素谱显著相关，而且与几种细菌类群和微生物衍生的植物雌激素代谢物的丰度也显著相关。总之，这些数据表明，除了对植物雌激素的雌激素受体敏感性的种间差异外，生殖结果可能还受到圈养 SWR 雌性肠道微生物群对饮食植物雌激素的转化的驱动。南部白犀牛（SWR）的偷猎活动达到了创纪录的水平，而圈养的不育使 SWR 保证种群不再能够自我维持。之前的研究已经确定饮食中的植物雌激素是造成这一问题的一个可能原因。在这里，我们通过比较两种犀牛物种来研究肠道微生物群在这一现象中的作用，这是首次对任何犀牛物种的肠道微生物群进行描述。据我们所知，我们的方法，结合平行测序、质谱分析和雌激素受体激活测定，为微生物介导的植物雌激素代谢与生育能力之间的关系提供了新的见解，这对于任何脊椎动物物种都是新颖的。有了这些信息，我们计划指导未来旨在提高圈养繁殖能力的工作，希望缓解它们灭绝的威胁。
