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

Abstract

Season has been suggested to contribute to variation in the gut microbiota of animals. The complicated relationships between amphibians and their gut microbiota and how they change throughout the year require more research. Short-term and long-term hypothermic fasting of amphibians may affect gut microbiota differently; however, these changes have not been explored. In this study, the composition and characteristics of the gut microbiota of Rana amurensis and Rana dybowskii during summer, autumn (short-term fasting) and winter (long-term fasting) were studied by high-throughput Illumina sequencing. Both frog species had higher gut microbiota alpha diversity in summer than autumn and winter, but no significant variations between autumn and spring. The summer, autumn, and spring gut microbiotas of both species differed, as did the autumn and winter microbiomes. In summer, autumn and winter, the dominant phyla in the gut microbiota of both species were Firmicutes, Proteobacteria, Bacteroidetes, and Actinobacteria. All animals have 10 OTUs (>90% of all 52 frogs). Both species had 23 OTUs (>90% of all 28 frogs) in winter, accounting for 47.49 ± 3.84% and 63.17 ± 3.69% of their relative abundance, respectively. PICRUSt2 analysis showed that the predominant functions of the gut microbiota in these two Rana were focused on carbohydrate metabolism, Global and overview maps, Glycan biosynthesis metabolism, membrane transport, and replication and repair, translation. The BugBase analysis estimated that among the seasons in the R. amurensis group, Facultatively_Anaerobic, Forms_Biofilms, Gram_Negative, Gram_Positive, Potentially_Pathogenic were significantly different. However, there was no difference for R. dybowskii. The research will reveal how the gut microbiota of amphibians adapts to environmental changes during hibernation, aid in the conservation of endangered amphibians, particularly those that hibernate, and advance microbiota research by elucidating the role of microbiota under various physiological states and environmental conditions.

Microbial communities are thermally more sensitive in warm-climate lizards compared with their cold-climate counterparts

“…The relative abundances of putative pathogens did not differ significantly among three temperature treatments in L. reevesii , but were enriched in P. przewalskii acclimated to 20°C. The accelerated colonization of pathogenic bacteria in the gut at low temperatures has been observed in other cold-climate vertebrates ( Liu et al, 2022 ; Tong et al, 2023 ). Bacteria of the genus Akkermansia can enhance metabolic homeostasis and anti-inflammatory properties ( Everard et al, 2013 ; Shin et al, 2014 ).…”

The Research Progress on the Interaction between Mammalian Gut Microbiota and the Host’s Metabolism Homeostasis during Hibernation

“…Due to the fasting behavior during hibernation, the scarcity of dietary substrates leads to a reduction or even disappearance of certain microbial groups that cannot adapt to extreme conditions [ 9 ]. Only a small fraction of these groups possess the ability to switch metabolic substrates or metabolize host-derived substrates during hibernation [ 23 ], enabling them to survive in this period.…”

“…During hibernation, alterations in the host’s food composition and shifts in the surrounding environment can significantly impact gut microbiota. Concurrently, these changes can have profound effects on the physiology of hibernating host animals [ 9 ]. Current research suggests that the interaction between the host and the gut microbiota during hibernation may be a critical factor, enabling hibernating animals to maintain homeostasis [ 10 , 11 , 12 ].…”

Gut microbiome diversity and function during hibernation and spring emergence in an aquatic frog

“…Although a considerable amount of research has been conducted on endothermic ('warm-blooded') animals, there exists a significant knowledge gap concerning ectothermic ('cold-blooded') species, such as amphibians, fish, and insects [11]. Among ectotherms, amphibians-and frogs, in particular-present a compelling case for the study of gut microbial dynamics [12,13]. Frogs are especially sensitive to environmental changes and possess a complex life history, making them exceptional models for research on gut microbiota [14].…”

“…During hibernation, frogs experience a sharp decline in metabolic rates and cease feeding activities, thereby entering a state of prolonged fasting [17]. These physiological adjustments could have farreaching consequences on their gut microbiota [13]. Moreover, the life stages of frog postmetamorphosis-juveniles and adults-differ in their energy investments; juveniles prioritize growth, while adults focus on reproduction [18,19].…”