Adapting to Novel Environments Together: Evolutionary and Ecological Correlates of the Bacterial Microbiome of the World's Largest Cavefish Diversification (Cyprinidae, Sinocyclocheilus).

Shipeng Zhou,Jayampathi Herath,Yewei Liu,Jian Yang,Tingru Mao,Gajaba Ellepola,Amrapali P Rajput,Madhava Meegaskumbura

doi:10.3389/fmicb.2022.823254

Shipeng Zhou, Jayampathi Herath + Show 6 more

Open Access

https://doi.org/10.3389/fmicb.2022.823254

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Abstract

The symbiosis between a host and its microbiome is essential for host fitness, and this association is a consequence of the host’s physiology and habitat. Sinocyclocheilus, the largest cavefish diversification of the world, an emerging multi-species model system for evolutionary novelty, provides an excellent opportunity for examining correlates of host evolutionary history, habitat, and gut-microbial community diversity. From the diversification-scale patterns of habitat occupation, major phylogenetic clades (A–D), geographic distribution, and knowledge from captive-maintained Sinocyclocheilus populations, we hypothesize habitat to be the major determinant of microbiome diversity, with phylogeny playing a lesser role. For this, we subject environmental water samples and fecal samples (representative of gut-microbiome) from 24 Sinocyclocheilus species, both from the wild and after being in captivity for 6 months, to bacterial 16S rRNA gene profiling using Illumina sequencing. We see significant differences in the gut microbiota structure of Sinocyclocheilus, reflective of the three habitat types; gut microbiomes too, were influenced by host-related factors. There is no significant association between the gut microbiomes and host phylogeny. However, there is some microbiome related structure at the clade level, with the most geographically distant clades (A and D) being the most distinct, and the two overlapping clades (B and C) showing similarities. Microbes inhabiting water were not a cause for significant differences in fish-gut microbiota, but water quality parameters were. Transferring from wild to captivity, the fish microbiomes changed significantly and became homogenized, signifying plastic changes and highlighting the importance of environmental factors (habitat) in microbiome community assembly. The core microbiome of this group, at higher taxonomic scale, resembled that of other teleost fishes. Our results suggest that divergent natural environments giving rise to evolutionary novelties underlying host adaptations, also includes the microbiome of these fishes.

Highlights

The gastrointestinal tract of an animal is occupied by a microbiome, a staggering diversity of microbial colonies that are in a symbiotic association with the host (Hooper and Gordon, 2001)
We collected 24 species of Sinocyclocheilus from the wild, together with their fecal samples and water samples from their habitat, they were raised in captivity (Figure 1)
The results revealed that the intestinal microbiota of the wild and captive groups divided along the first MDS axis into two distinct clusters: the cluster of captives was more cohesive (Figure 5B), indicating that captivity altered cavefish gut microbiota and, to a certain extent, homogenized the gut bacteria across species

Summary

Introduction

The gastrointestinal tract of an animal is occupied by a microbiome, a staggering diversity of microbial colonies that are in a symbiotic association with the host (Hooper and Gordon, 2001). These commensal gut-bacterial relationships influence many vital aspects of the host, such as immune function, nutrient absorption, development, and behavior (Mazmanian et al, 2005; Nicholson et al, 2005; Mcfall-Ngai et al, 2013). The microbiome of a host is dynamic system (Talwar et al, 2018), where microbe communities change depending on the environment and host physiology (Nayak, 2010). Large diversification-scale studies addressing correlates of host evolutionary history and microbial community diversity are few (Ross et al, 2018)

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