Kinship, inbreeding and fine‐scale spatial structure influence gut microbiota in a hindgut‐fermenting tortoise

Abstract

Herbivorous vertebrates rely on complex communities of mutualistic gut bacteria to facilitate the digestion of celluloses and hemicelluloses. Gut microbes are often convergent based on diet and gut morphology across a phylogenetically diverse group of mammals. However, little is known about microbial communities of herbivorous hindgut-fermenting reptiles. Here, we investigate how factors at the individual level might constrain the composition of gut microbes in an obligate herbivorous reptile. Using multiplexed 16S rRNA gene sequencing, we characterized the faecal microbial community of a population of gopher tortoises (Gopherus polyphemus) and examined how age, genetic diversity, spatial structure and kinship influence differences among individuals. We recovered phylotypes associated with known cellulolytic function, including candidate phylum Termite Group 3, suggesting their importance for gopher tortoise digestion. Although host genetic structure did not explain variation in microbial composition and community structure, we found that fine-scale spatial structure, inbreeding, degree of relatedness and possibly ontogeny shaped patterns of diversity in faecal microbiomes of gopher tortoises. Our findings corroborate widespread convergence of faecal-associated microbes based on gut morphology and diet and demonstrate the role of spatial and demographic structure in driving differentiation of gut microbiota in natural populations.

Physically Effective Fiber Threshold, Apparent Digestibility, and Novel Fecal Microbiome Identification of the Leopard Tortoise (Stigmochelys pardalis)

“…Although present, methane production has been demonstrated to be much less in the cecum of hindgut-fermenting rats, compared to the rumen of foregut-fermenting cattle, due to a higher affinity for the use of H2 to reduce CO2 into acetate (Miller and Wolin, 1979 (Yuan et al, 2015).…”

“…The next abundant phylum in these individuals was Bacteroidetes, although it paled in comparison to Firmicutes, ranging from 4.2 to 10.1% of OTUs (Hong et al, 2011). Conversely, Yuan et al (2015) Table 12. Fecal archaea and bacterial microbial OTU contributions of free-ranging herbivorous, hindgut-fermenting reptiles.…”

“…The hydrolysis of starch components (amylose, amylopectin, and glycogen) yields glucose and maltose (Sharp et al, 1989); maltose can be further digested, while glucose can enter the fermentation cycle and produce SCFAs. Members of Bacilli have been identified as amylolytic, and although unspecified, Bacilli has been identified in the fecal microbiome of G. polyphemus (Yuan et al, 2015).…”

“…Ethanol, a by-product of cellulose fermentation, can also be used as a substrate for acetate production (Andreesen et al, 1989). The cellulolytic Clostridia families Ruminococcaceae, Lachnospiraceae, Christensenellaceae, Clostridiaceae, Clostridiaceae and Synthrophomonadaceae, as well as the Bacilli order Bacteroidiales (Bacteroidetes) have been identified in the fecal microbiome of G. polyphemus (Yuan et al, 2015).…”

“…Fecal bacterial phyla of leopard tortoises fed a pelleted herbivorous tortoise diet (CNTRL, n = 4), the same diet with added 2.0 mm (2.0 mm, n = 6) or 0.2 mm length cellulose fiber (0.2 mm, n = 6), and free-ranging gopher tortoises (Gaillard, 2014;Yuan et al, 2015).…”