Abstract
As a natural hibernator, the Chinese alligator (Alligator sinensis) is an ideal and intriguing model to investigate changes in microbial community structure and function caused by hibernation. In this study, we used 16S rRNA profiling and metagenomic analysis to compare the composition, diversity, and functional capacity in the gut microbiome of hibernating vs. active Chinese alligators. Our results show that gut microbial communities undergo seasonal restructuring in response to seasonal cycles of feeding and fasting in the Chinese alligator, but this animal harbors a core gut microbial community primarily dominated by Proteobacteria, Fusobacteria, Bacteroidetes, and Firmicutes across the gut regions. During hibernation, there is an increase in the abundance of bacterial taxa (e.g., the genus Bacteroides) that can degrade host mucin glycans, which allows adaptation to winter fasting. This is accompanied by the enrichment of mucin oligosaccharide-degrading enzyme and carbohydrate-active enzyme families. In contrast, during the active phase (feeding), active Chinese alligators exhibit a carnivore gut microbiome dominated by Fusobacteria, and there is an increase in the relative abundance of bacteria (e.g., Cetobacterium somerae) with known proteolytic and amino acids-fermentating functions that improve host protein-rich food digestion efficiency. In addition, seasonal variations in the expression of β-defensins play a protective role in intestinal immunity. These findings provide insights into the functional adaptations of host–gut microbe symbioses to seasonal dietary shifts to maintain gut homeostasis and health, especially in extreme physiological states.
Highlights
The animal gastrointestinal (GI) tract harbors diverse and complex microbial ecosystems that profoundly affect numerous aspects of host biology (Jandhyala et al, 2015), including nutrient extraction (Shortt et al, 2018), development of the immune system (Thaiss et al, 2016), and resistance to invading pathogens (Ouwerkerk et al, 2013)
Microbial community composition showed seasonal variations, with the phylum Fusobacteria detected at a high level from the duodenum to feces in active alligators, and the phylum Bacteroidetes being more abundant during hibernation than during the active state, in the feces (Supplementary Table S4)
The predominant lineages in the gut of hibernating alligator was more diverse at the species level (Supplementary Table S11) than those observed during the feeding state, which may contribute to the higher diversity during hibernation
Summary
The animal gastrointestinal (GI) tract harbors diverse and complex microbial ecosystems that profoundly affect numerous aspects of host biology (Jandhyala et al, 2015), including nutrient extraction (Shortt et al, 2018), development of the immune system (Thaiss et al, 2016), and resistance to invading pathogens (Ouwerkerk et al, 2013). The Chinese alligator (Alligator sinensis) is an ancient, endangered and endemic freshwater crocodilian that was listed as a first-class protected species by the Chinese government in 1972 (Thorbjarnarson and Xiaoming, 1999). It was listed as a critically endangered species in the International Union for Conservation of Nature and Natural Resources (IUCN) Red List (Zhang et al, 2016). The Chinese alligator is a poikilotherm whose body temperature (Tb) varies with the ambient temperature It completely ceases food intake and body movement and enters a state of hibernation when the environmental temperature falls below 14◦C (Zhang et al, 2017). The Chinese alligator is not interrupted by spontaneous periodic arousals, which are characteristic of the 13-lined ground squirrel (Stevenson et al, 2014)
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