Dataset Information

The role of the gut microbiota in the dietary niche expansion of fishing bats

ABSTRACT:

Background

Due to its central role in animal nutrition, the gut microbiota is likely a relevant factor shaping dietary niche shifts. We analysed both the impact and contribution of the gut microbiota to the dietary niche expansion of the only four bat species that have incorporated fish into their primarily arthropodophage diet.

Results

We first compared the taxonomic and functional features of the gut microbiota of the four piscivorous bats to that of 11 strictly arthropodophagous species using 16S rRNA targeted amplicon sequencing. Second, we increased the resolution of our analyses for one of the piscivorous bat species, namely Myotis capaccinii, and analysed multiple populations combining targeted approaches with shotgun sequencing. To better understand the origin of gut microorganisms, we also analysed the gut microbiota of their fish prey (Gambusia holbrooki). Our analyses showed that piscivorous bats carry a characteristic gut microbiota that differs from that of their strict arthropodophagous counterparts, in which the most relevant bacteria have been directly acquired from their fish prey. This characteristic microbiota exhibits enrichment of genes involved in vitamin biosynthesis, as well as complex carbohydrate and lipid metabolism, likely providing their hosts with an enhanced capacity to metabolise the glycosphingolipids and long-chain fatty acids that are particularly abundant in fish.

Conclusions

Our results depict the gut microbiota as a relevant element in facilitating the dietary transition from arthropodophagy to piscivory.

Supplementary Information

The online version contains supplementary material available at 10.1186/s42523-021-00137-w.

SUBMITTER: Aizpurua O

PROVIDER: S-EPMC8555116 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:Plasticity in the microbial community composition and function can permit the host to adapt to ecological, environmental, and physiological changes. Much of the information on the gut microbiota-host relationship to date derives from studies of laboratory model organisms, while little is known concerning wild animals and their ecological relevance to gut microbes. It is also unclear how microbial community composition and activity adapt to changes in diet and energy, nutritional requirements, and utilization induced by dietary expansion from invertebrates to vertebrates. The great evening bat (Ia io) is both an insectivore and an avivore (that is, a bird-eater), and thus provides an opportunity to investigate the diet-host-microbiota-physiology relationship. Here, we investigated this relationship by using 16S rRNA amplicon sequencing and functional prediction in adult males of I. io. We found that gut microbial diversity was similar, while microbial community structures were significantly different between insectivorous and avivorous diets. Moreover, increases in the relative abundance of Firmicutes and the Firmicutes-to-Bacteroidetes ratio, changes in carbohydrate and nucleotide metabolism, and a decrease in Pseudomonas were associated with higher energy demands for hunting birds and with fat storage for entering hibernation and migration. These findings demonstrated that seasonal dietary shifts drive a significant change in the composition and function of gut microbiomes, thereby facilitating adaptation to the challenging avian dietary niche in bats. These results suggest that the gut microbial communities can constantly respond to alterations in diets, potentially facilitating the diversity of wild animal dietary niches, and enhance our understanding of the diet-host-microbiota-physiology relationship. IMPORTANCE The coevolution between the host and its gut microbes can promote an animal's adaptation to its specific ecological niche and changes in energy and nutritional requirements. This study focused on an avivorous bat, the great evening bat (Ia io), to investigate how seasonal dietary shifts affect the gut microbial composition and function, thereby facilitating adaptation to an avian diet. We found that seasonal dietary shifts driving a significant change in the composition and function of gut microbiomes in I. io were associated with higher energy demands for hunting birds and fat storage for entering hibernation and migration. Our study provides novel insight into the role of gut bacteria in generating ecological diversity and flexibility in wild mammals. The results are valuable for clarifying the complicated host-microbiota-physiology relationship in a dietary niche expansion context.

Project description:BackgroundDietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25-35 kg/m2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers.ResultsAX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.ConclusionThis study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.Trial registrationClinicaltrials.gov, NCT02322112 , registered on July 3, 2015. Video Abstract.