Abstract

The hologenome concept proposes that microbes and their host organism are an independent unit of selection. Motivated by this concept, we hypothesized that thermal acclimation in poikilothermic organisms, owing to their inability to maintain their body temperature, is connected to their microbiome composition. To test this hypothesis, we used a unique experimental setup with a transgenerational selective breeding scheme for cold tolerance in tropical tilapias. We tested the effects of the selection on the gut microbiome and on host transcriptomic response. Interestingly, we found that host genetic selection for thermal tolerance shapes the microbiome composition and its response to cold. The microbiomes of cold-resistant fish showed higher resilience to temperature changes, indicating that the microbiome is shaped by its host's selection. These findings are consistent with the hologenome concept and highlight the connection between the host and its microbiome's response to the environment.

Highlights

  • Cold temperature is an environmental challenge that greatly affects metabolic and physiological processes

  • Our results suggest that host selection for cold tolerance is followed by changes in the gut microbiome, which are manifested by higher resilience to temperature shifts and which may be a key factor in orchestrating cold acclimation in poikilothermic animals

  • Our insight into the microbial dynamics of the blue tilapia gut microbiome in response to environmental conditions shows that temperature, host genetic background and tolerance to thermal stress are major determinants of community structure and dynamics

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Summary

Introduction

Cold temperature is an environmental challenge that greatly affects metabolic and physiological processes. The universality of host–microbe associations, either transient or tight, inspired the hologenome concept (Bordenstein and Theis, 2015; Brucker and Bordenstein, 2013; Rosenberg and Zilber-Rosenberg, 2013; Rosenberg and Zilber-Rosenberg, 2016; Rosenberg and Zilber-Rosenberg, 2018; Theis et al, 2016), which proposes that within the holobiont, units at different levels, such as genes, chromosomes or biont combinations (i.e., host and microbes), are subject to selection or neutrality Within this concept, host–microbe interactions have an important role in the host’s physiology, whilst microbiome composition may be affected by host selection. We hypothesized that host selection may facilitate changes in the host-associated microbial species and in their response to environmental selection pressure

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