Variation in gut microbiome structure across the annual hibernation cycle in a wild primate

Abstract

The gut microbiome can mediate host metabolism, including facilitating energy-saving strategies like hibernation. The dwarf lemurs of Madagascar (Cheirogaleus spp.) are the only obligate hibernators among primates. They also hibernate in the subtropics, and unlike temperate hibernators, fatten by converting fruit sugars to lipid deposits, torpor at relatively warm temperatures, and forage for a generalized diet after emergence. Despite these ecological differences, we might expect hibernation to shape the gut microbiome in similar ways across mammals. We, therefore, compare gut microbiome profiles, determined by amplicon sequencing of rectal swabs, in wild furry-eared dwarf lemurs (C. crossleyi) during fattening, hibernation, and after emergence. The dwarf lemurs exhibited reduced gut microbial diversity during fattening, intermediate diversity and increased community homogenization during hibernation, and greatest diversity after emergence. The Mycoplasma genus was enriched during fattening, whereas the Aerococcaceae and Actinomycetaceae families, and not Akkermansia, bloomed during hibernation. As expected, the dwarf lemurs showed seasonal reconfigurations of the gut microbiome; however, the patterns of microbial diversity diverged from temperate hibernators, and better resembled the shifts associated with dietary fruits and sugars in primates and model organisms. Our results thus highlight the potential for dwarf lemurs to probe microbiome-mediated metabolism in primates under contrasting conditions.

Short Photoperiod-Dependent Enrichment of Akkermansia spec. as the Major Change in the Intestinal Microbiome of Djungarian Hamsters (Phodopus sungorus)

“…Although this analytic strategy excluded taxonomic units identified to only phylum, class, or order level, the diversity estimated via the Shannon Index was comparable to earlier data from this species [ 15 , 18 ]. As in other studies from rodents and primates [ 19 , 20 , 21 , 22 , 23 ], Firmicutes and Bacteroidetes were the most abundant phyla, although the relative amount of Bacteroidetes was lower in the hamsters of the present study [ 12 , 14 , 18 , 19 ]. Furthermore, the Ulm hamsters’ microbiome contained a similar amount of Proteobacteria when compared to other Djungarian hamsters and other rodents, ranging from 2 to 10% [ 12 , 14 , 18 , 20 , 21 , 24 , 25 ].…”

“…However, although Djungarian hamsters neither fasted nor overfed during short photoperiod acclimation, their microbiome showed an increase in Akkermansia abundance. Together with the fact that no Akkermansia blooming was detectable in seasonally hibernating carnivorous Brown bears ( Ursus arctos ) [ 46 ] or frugivorous furry-eared dwarf lemurs ( Cheirogaleus crossleyi ) [ 22 ], the results of the present study suggest a large variety of microbiome responses to a seasonally changing environment.…”

Characteristics and a comparison of the gut microbiota in two frog species at the beginning and end of hibernation

“…In the present study, the summer, autumn, and spring gut microbiotas of both species differed, as did the autumn (short-term fasting) and winter (long-term fasting) microbiomes. The effect of the seasons on the intestinal microbiota of animals has been studied extensively ( Weng et al, 2016 ; Wiebler et al, 2018 ; Xiao et al, 2019 ; Zhou et al, 2021 ; Fan et al, 2022 ; Greene et al, 2022 ). The intestinal microbiota of difference between short-term (weeks, autumn) and long-term (months, spring) fasting has rarely been examined, and there are numerous plausible explanations.…”

“…In the present study, alpha diversity fluctuated among seasons, but autumn and spring had no significant differences. Previous investigations of the gut microbiota of hibernating animals have yielded contradictory results in terms of alpha diversity (Weng et al, 2016;Wiebler et al, 2018;Xiao et al, 2019;Zhou et al, 2021;Fan et al, 2022;Greene et al, 2022), which may be due to several factors (such as diet, habitat and temperature). Diet has a significant impact on these communities, with both short-term dietary changes and long-term dietary patterns having an impact (Lee et al, 2020).…”

“…Season has been suggested to contribute to variation in the gut microbiota of animals ( Tang et al, 2019 ; Xiao et al, 2019 ; Huang and Liao, 2021 ; Zhou et al, 2021 ; Fan et al, 2022 ; Greene et al, 2022 ). Many environmental factors, such as temperature, diet, and habitat, among others, are responsible for these alterations ( Xiao et al, 2019 ; Huang and Liao, 2021 ; Zhou et al, 2021 ; Fan et al, 2022 ; Greene et al, 2022 ). Seasonal food availability affects amphibians’ gut microbiome ( Baniel et al, 2021 ).…”