Clinical health issues, reproductive hormones, and metabolic hormones associated with gut microbiome structure in African and Asian elephants

Abstract

Background The gut microbiome is important to immune health, metabolism, and hormone regulation. Understanding host–microbiome relationships in captive animals may lead to mediating long term health issues common in captive animals. For instance, zoo managed African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) experience low reproductive rates, high body condition, and gastrointestinal (GI) issues. We leveraged an extensive collection of fecal samples and health records from the Elephant Welfare Study conducted across North American zoos in 2012 to examine the link between gut microbiota and clinical health issues, reproductive hormones, and metabolic hormones in captive elephants. We quantified gut microbiomes of 69 African and 48 Asian elephants from across 50 zoos using Illumina sequencing of the 16S rRNA bacterial gene. Results Elephant species differed in microbiome structure, with African elephants having lower bacterial richness and dissimilar bacterial composition from Asian elephants. In both species, bacterial composition was strongly influenced by zoo facility. Bacterial richness was lower in African elephants with recent GI issues, and richness was positively correlated with metabolic hormone total triiodothyronine (total T3) in Asian elephants. We found species-specific associations between gut microbiome composition and hormones: Asian elephant gut microbiome composition was linked to total T3 and free thyroxine (free T4), while fecal glucocorticoid metabolites (FGM) were linked to African elephant gut microbiome composition. We identified many relationships between bacterial relative abundances and hormone concentrations, including Prevotella spp., Treponema spp., and Akkermansia spp. Conclusions We present a comprehensive assessment of relationships between the gut microbiome, host species, environment, clinical health issues, and the endocrine system in captive elephants. Our results highlight the combined significance of host species-specific regulation and environmental effects on the gut microbiome between two elephant species and across 50 zoo facilities. We provide evidence of clinical health issues, reproductive hormones, and metabolic hormones associated with the gut microbiome structure of captive elephants. Our findings establish the groundwork for future studies to investigate bacterial function or develop tools (e.g., prebiotics, probiotics, dietary manipulations) suitable for conservation and zoo management.

Comparison of the gut microbiome and resistome in captive African and Asian elephants on the same diet

“…Four bacterial phyla are core members of the mammalian gut microbiome including Bacteroidetes, Firmicutes, Proteobacteria and Actinobacteria ( 51 ). Consistent with previous research findings ( 5 , 12 , 52 , 53 ), our results showed the gut microbiome of captive African and Asian elephants was dominated by two phyla: Bacteroidetes and Firmicutes , following by Spirochaetes, Verrucomicrobia and Protrobacteria ( Figures 2A , B ). Compared to dominant phyla in other animals like cow ( Clostridiales and Prevotellaceae ) or termite ( Spirochetes and Fibrobacteres ), the dominant phyla in elephants allow them digest various plant biopolymers ( 9 , 54 ).…”

“…In our study, African and Asian elephants had different gene abundance patterns. This also has been shown previously by Keady et al ( 12 ) that African and Asian elephants have different microbial structure and dissimilar bacterial composition ( 12 ). The difference was mainly caused by the host species as the PERMANOVA analysis showed that the host species explained 63% of the variation.…”

“…Health issues common in captive animals may be closely related to the gut microbiome ( 10 ). Interventions of gut microbiome may serve as a feasible approach to improve health, survival and reproductive rate of captive elephants ( 11 , 12 ). In order to develop more effective management strategies to improve the survival of captive elephants, information on their basic biology such as their gut microbiome is needed.…”

Taxonomic and metabolic diversity of Actinobacteria isolated from faeces of a 28,000-year-old mammoth

“…Furthermore, Actinobacteria represent only a very minor fraction of the mammalian gut, in particular when compared to soil samples; still, antibiotic-producing Actinobacteria have been isolated from the faeces of a variety of mammals [39][40][41] . Studies analysing the microbiome composition of elephants, the closest living relative to mammoths, report the presence of actinobacterial reads in low abundance, including Streptomyces, Sanguibacter, Micromonospora and Saccharopolyspora, but not Oerskovia [42][43][44] . Species of Streptomyces and Micromonospora have been isolated from the faeces of elephants 41,45 .…”

Fecal microbiota transplants modulate the gut microbiome of a two‐toed sloth (Choloepus didactylus)

“…We conducted 16 S rRNA gene amplicon library preparation of the V4−V5 region as specified in Keady et al (2021) and sequenced the final 4 nM library on an Illumina MiSeq with a 2 × 300 bp v3 kit.…”