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.

Keywords: Chiroptera; Diet; Microbiome; Microorganism; Niche shift; Piscivorous; Trophic niche.

Fig. 1

Map of the approximate distributional range (latitude and longitude limits) of bats analysed in this study (left), and species and number of individuals (n) used in each step of the analysis (right). In the first step, 37 bats from four well-known fish-consuming colonies of the four piscivorous species were compared to 47 bats belonging to 11 strict arthropodophagous species. In the second step, we increased the resolution of the analyses in the piscivorous bat Myotis capaccinii, by adding more individuals (n = 15) from three allegedly non-piscivorous colonies to the analysis. For these analyses we also included arthropodophagous bats that roost in the same cave as the piscivorous M. capaccinii, namely Miniopterus schreibersii and Myotis myotis as controls

Fig. 2

Differentially abundant amplicon sequence variants (ASVs) between piscivorous and arthropodophagous bats displayed at the bacterial genus level. Only ASVs with a significance value of p < 0.01 are shown. Positive values indicate genera that were enriched in piscivorous bats, while negative values show those enriched in arthropodophagous bats. Colours of the circles indicate phyla. Each circle represents a single ASV, thus multiple circles within a genus indicate multiple ASV that were enriched. The five highlighted bacterial genera are the ones that contributed the most to the ensemble predictive models of piscivorous bats

Fig. 3

Ordination of the gut microbial communities of the analysed bats. a Samples coloured by host species. b Samples coloured by taxonomic families. c Samples coloured according to the dietary groups set before the machine learning classification. Grey dots represent Myotis capaccinii individuals from colonies in which no piscivory has been reported. These samples were excluded from the machine learning model training process. d Samples coloured according to the dietary groups predicted by the machine learning classification. The green dot is the only M. capaccinii that was classified as an arthropodophage. The bat species abbreviations are Ebo = Eptesicus bottae, Har = Hypsugo ariel, Msc = Miniopterus schreibersii, Mca = Myotis capaccinii, Mda = M. daubentonii, Mem = M. emarginatus, Mmy = M. myotis, Mpi = M. pilosus, Mvi = M. vivesi, Nle = Noctilio leporinus, Pku = Pipistrellus kuhlii, Rbl = Rhinolophus blasii, Reu = R. euryale, Rhi = R. hipposideros, Rfe = R. ferrumequinum

Fig. 4

Relative abundance of the most relevant bacteria enriched in piscivorous or arthropodophagous bats in a the four piscivorous bat species, b Myotis capaccinii colonies in which no piscivory has been recorded so far, c the eleven arthropodophagous bats analysed, and d the eastern mosquitofish (G. holbrooki) consumed by piscivorous M. capaccinii

Fig. 5

a Cumulative relative representation of ASVs detected in fish guts measured in different groups of bats. b Relative representation of bacteria in the intestinal tracts of M. capaccinii and Gambusia. c Number of Aeromonas ASVs detected in M. capaccinii bats and Gambusia fish. d Depth of coverage of Aeromonas and ash3 (aerolysin precursor) gene recovered from bat shotgun metagenomes

Fig. 6

Differential abundance analysis of Piphillin predicted KEGG pathways of piscivory-associated microbial communities (left) and arthropodophagous-associated microbial communities (right) at the significance level of p < 0.01