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

Ostaizka Aizpurua,Orly Razgour,L Gerardo Herrera Montalvo,Aiqing Lin,M Thomas P Gilbert,Lasse Nyholm,Evie Morris,Antton Alberdi,Gloriana Chaverri,José Juan Flores-Martinez

doi:10.1186/s42523-021-00137-w

Abstract

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

Highlights

Due to its central role in animal nutrition, the gut microbiota is likely a relevant factor shaping dietary niche shifts
We increased the resolution of our analyses in the piscivorous bat Myotis capaccinii, by adding more individuals from three allegedly non-piscivorous colonies to the analysis, as well as incorporating shotgun sequencing data for direct fish DNA quantification and inference of functional microbiota features
We implemented an integrative approach that included Hill numbers-based diversity analyses [18], multivariate statistics, ensemble machine learning modelling [19] and enrichment analyses, in Piscivorous bats host unique gut microbiotas Taxonomic characterisation of the gut microbiota associated with the 15 bat species studied using amplicon sequencing exhibited an overall microbial community that was comprised of 27 phyla, which was principally dominated by Proteobacteria (56.36 ± 33.41%; mean ± standard deviation) and Firmicutes (22.16 ± 28.78%)

Summary

Introduction

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. While some bat species have specialised in consuming a single food resource (e.g. blood-feeding bats, [14]), others have incorporated new feeding resources into their ancestral arthropod-based diet [10], expanding their dietary niche One example of the latter is the case of the four well-known piscivorous ( known as fishing) bat species [15], which have independently developed fishing behaviour in four geographical areas across the planet (Fig. 1). Despite this fascinating twist to their life history, the spatio-temporal patterns, causes and consequences of fishing behaviour largely remain unexplored

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