Dataset Information

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros.

ABSTRACT: With recent poaching of southern white rhinoceros (SWR [Ceratotherium simum simum]) 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 [Rhinoceros unicornis]), 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 in vitro 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.IMPORTANCE 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.

SUBMITTER: Williams CL

PROVIDER: S-EPMC6456749 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros.

Williams Candace L CL Ybarra Alexis R AR Meredith Ashley N AN Durrant Barbara S BS Tubbs Christopher W CW

mBio 20190409 2

With recent poaching of southern white rhinoceros (SWR [<i>Ceratotherium simum simum</i>]) 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 ...[more]

PMID: 30967461

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Project description:All species in the extant Rhinocerotidae family are experiencing increased threats in the wild, making captive populations essential genetic reservoirs for species survival. However, managed species face distinct challenges in captivity, resulting in populations that are not self-sustaining. Captive southern white rhinoceros (Ceratotherium simum simum) have low reproductive rates and presumed acyclicity is common among females. Although many females fail to ovulate, follicle growth may occur and ovulation can be hormonally induced. Female southern white rhino (n = 6), housed as a bachelorette group, were determined to be ovulatory (n = 1) or anovulatory (n = 5) by serial ultrasound and fecal progestagen analysis. When follicles reached pre-ovulatory size (~35 mm), females (n = 4) were induced to ovulate in 11 trials with a GnRH analog (4.5 mg, SucroMate™) via single intramuscular injection. Nine trials resulted in ovulation (81.8%), all between 36 and 48 hours post-treatment. Ovulations were confirmed by progestagen elevation above baseline coincident with visualization of a corpus luteum (CL). Luteal phases were characterized as short (<50 days) or long (≥50 days). Between short and long cycles, only the number of days of progestagen above baseline was significantly different (P < 0.05), while days with visible luteal structures was not significant (P = 0.11). Both cycle types were observed following both spontaneous and induced ovulations. Furthermore, we showed that longer cycle lengths do not necessarily indicate early pregnancy loss as none of the females were bred or inseminated during the study. While anovulation is common in the southern white rhino captive population, ovulation induction can be achieved efficiently and predictably for use in conjunction with artificial insemination or to facilitate natural breeding. This information will lead to more efficient use of assisted reproductive technologies to overcome reproductive challenges in this species and to generate genetically healthy captive populations as a hedge against extinction.

Project description:Gut microbiota are essential to nutrient metabolism and the maintenance of hindgut health. The characterization of faecal bacterial communities from healthy individuals is important for the establishment of baseline data that can be compared to periods of gut dysbiosis. Diet is a key determinant of the faecal microbial community structure and generation of volatile fatty acids, a main energy source for the host. While rhinoceroses are herbivores, black rhinoceroses are browsers and white rhinoceroses are grazers. The objective of our study was to characterize and compare diets, faecal bacterial communities, nutrients and metabolites between and amongst Southern white rhinoceroses and Southern black rhinoceroses (n = 3 rhinos/species) managed at Disney's Animal Kingdom® . Faecal bacterial communities were similar between individual white rhinos and dissimilar between species and individual black rhinos. Faecal butyrate and propionate molar proportions and concentrations were greater in black rhinos than white rhinos, whereas lactate was greater in white rhinos. The Shannon diversity, total operational taxonomic units, and relative abundance of Firmicutes were greater in white than black rhinos. The relative abundance of Proteobacteria in faeces from black rhinos was 3-fold greater than from white rhinos. One black rhino had a greater relative abundance of Verrucomicrobia (7.45 ± 1.31%) than all other individual rhinos (0.01-1.37%). White rhinoceroses demonstrated similar abundances of bacterial phyla and communities between one another and by individual, while black rhinoceroses were more dissimilar by individual. The dissimilarities between black rhinos were suspected to be due to total diet consumption variability, including browse diversity, and lack of direct contact. In contrast, the white rhinos commingled (i.e. nose-to-nose contact) and consumed similar amounts of hay, pellets and training items. These results suggest that species-specific diets and the individual contribute to differences in faecal bacterial communities, nutrients and metabolites between black and white rhinos housed at the same institution.

Project description:BackgroundManaged southern white rhinoceros (Ceratotherium simum simum) serve as assurance populations for wild conspecifics threatened by poaching and other anthropocentric effects, though many managed populations experience subfertility and reproductive failure. Gut microbiome and host health are inextricably linked, and reproductive outcomes in managed southern white rhinoceros may be mediated in part by their diet and gut microbial diversity. Thus, understanding microbial dynamics within managed populations may help improve conservation efforts. We characterized the taxonomic composition of the gut microbiome in the managed population of female southern white rhinoceros (n = 8) at the North Carolina Zoo and investigated the effects of seasonality (summer vs. winter) and age classes (juveniles (n = 2; 0-2 years), subadults (n = 2; 3-7 years), and adults (n = 4; >7 years)) on microbial richness and community structure. Collection of a fecal sample was attempted for each individual once per month from July-September 2020 and January-March 2021 resulting in a total of 41 samples analyzed. Microbial DNA was extracted and sequenced using the V3-V4 region of the 16S rRNA bacterial gene. Total operational taxonomic units (OTUs), alpha diversity (species richness, Shannon diversity), and beta diversity (Bray-Curtis dissimilarity, linear discriminant analysis effect size) indices were examined, and differentially enriched taxa were identified.ResultsThere were differences (p < 0.05) in alpha and beta diversity indices across individuals, age groups, and sampling months. Subadult females had higher levels of Shannon diversity (Wilcoxon, p < 0.05) compared to adult females and harbored a community cluster distinct from both juveniles and adults. Samples collected during winter months (January-March 2021) possessed higher species richness and statistically distinct communities compared to summer months (July-September 2020) (PERMANOVA, p < 0.05). Reproductively active (n = 2) and currently nonreproductive adult females (n = 2) harbored differentially enriched taxa, with the gut microbiome of nonreproductive females significantly enriched (p = 0.001) in unclassified members of Mobiluncus, a genus which possesses species associated with poor reproductive outcomes in other animal species when identified in the cervicovaginal microbiome.ConclusionTogether, our results increase the understanding of age and season related microbial variation in southern white rhinoceros at the North Carolina Zoo and have identified a potential microbial biomarker for reproductive concern within managed female southern white rhinoceros.

Dataset Information

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros.

Publications

Gut Microbiota and Phytoestrogen-Associated Infertility in Southern White Rhinoceros.

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