Abstract

BackgroundHost microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition and reproductive output may allow for the development of microbial augmentation strategies to improve success. Here, we characterise faecal bacterial communities of breeding and non-breeding eastern black rhino (Diceros bicornis michaeli) using 16S rRNA gene amplicon sequencing and quantify progestagen and glucocorticoid metabolite concentrations through enzyme immunoassays to identify such relationships.ResultsWe identified significant differences in black rhino gut microbiome composition according to ID, institution, breeding success and ovarian cycle phase. In particular, the gut microbiome during pregnancy and post-parturition was significantly altered. Around a third of bacterial genera showed more than ± 10% correlation with either progestagen and/or glucocorticoid concentration, and in general, microbial genera correlated with both hormones in the same direction. Through a combination of analyses, we identified four genera (Aerococcaceae, Atopostipes, Carnobacteriaceae and Solobacterium) that were significantly associated with breeding success, pregnancy and/or post-parturition, and higher faecal progestagen metabolite concentrations. These genera had a lower-than-average relative abundance in the gut microbiome.ConclusionOur results indicate that many members of the gut microbiome of black rhino are associated with hormone production and breeding success, and some members of the rare microbiota appear to be particularly important. Although the directionality of the relationship is unclear, the variation in gut microbiome communities represents a potential biomarker of reproductive health. We identified four genera that were associated with multiple indicators of reproductive output; these could be candidate probiotics to improve the breeding success of black rhino in zoo-based conservation breeding programmes. Further work is required to understand the efficacy and feasibility of this, either directly through microbial augmentation (e.g. probiotics) or indirectly via dietary manipulation or prebiotics.

Highlights

  • Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms

  • Indicator analysis identified seven genera with significantly different abundance in rhino gut microbiomes according to breeding success: five that were more abundant in breeding rhino and two that were more so in non-breeding rhino (Table 1)

  • We show that progestagen and glucocorticoid metabolites are correlated in black rhino, and find evidence that both glucocorticoids and progestagens are higher during the luteal phase than the follicular phase, and both are much higher during pregnancy

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Summary

Introduction

Host microbiomes play a role in hormone production and subsequent fertility in humans, but this is less well understood in non-model organisms. This is of particular relevance to species in zoo-based conservation breeding programmes, as relationships between host microbiome composition and reproductive output may allow for the development of microbial augmentation strategies to improve success. Host-associated microbial communities (“microbiomes”) play a critical role in influencing a diverse suite of whole-organism functions, with classic examples including immunity and metabolism [1–4]. The gut microbiota can produce endocrine molecules including biologically active catecholamines (norepinephrine and dopamine) [13], and the gut microbiota can degrade hormones and change host gene expression, with consequences for reproductive success [14]. The microbiome of the reproductive tract can affect a range of pregnancy outcomes for humans, and research is ongoing to understand how the microbiome could be manipulated to improve pregnancy rates and completion to term [18–20]

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