Defining Coral Bleaching as a Microbial Dysbiosis within the Coral Holobiont.

Caroline E Dubé,Alexandre Mercière,Cécile Gruet,Nicolas Derome,Aurélie Boilard,Alejandra Hernandez-Agreda

doi:10.3390/microorganisms8111682

Abstract

Coral microbiomes are critical to holobiont health and functioning, but the stability of host–microbial interactions is fragile, easily shifting from eubiosis to dysbiosis. The heat-induced breakdown of the symbiosis between the host and its dinoflagellate algae (that is, “bleaching”), is one of the most devastating outcomes for reef ecosystems. Yet, bleaching tolerance has been observed in some coral species. This review provides an overview of the holobiont’s diversity, explores coral thermal tolerance in relation to their associated microorganisms, discusses the hypothesis of adaptive dysbiosis as a mechanism of environmental adaptation, mentions potential solutions to mitigate bleaching, and suggests new research avenues. More specifically, we define coral bleaching as the succession of three holobiont stages, where the microbiota can (i) maintain essential functions for holobiont homeostasis during stress and/or (ii) act as a buffer to mitigate bleaching by favoring the recruitment of thermally tolerant Symbiodiniaceae species (adaptive dysbiosis), and where (iii) environmental stressors exceed the buffering capacity of both microbial and dinoflagellate partners leading to coral death.

Highlights

Coral reefs are one of the most biologically diverse and economically important marine ecosystems on the planet
Coral bleaching is the result of the breakdown of the obligate symbiosis between the coral animal and its photosynthetic dinoflagellate endosymbionts [38], leading to the white calcium carbonate skeleton being visible through the transparent host tissue (Figure 1)
Given the key roles exerted by the microbiota and the Symbiodiniaceae in maintaining the host’s health and homeostasis [54,55,56], numerous studies have investigated the mechanisms by which these symbiotic partners can mitigate coral bleaching and increase resilience of the coral holobiont to other climate related stressors [36,57,58]

Summary

Introduction

Coral reefs are one of the most biologically diverse and economically important marine ecosystems on the planet. Coral bleaching is the result of the breakdown of the obligate symbiosis between the coral animal and its photosynthetic dinoflagellate endosymbionts [38], leading to the white calcium carbonate skeleton being visible through the transparent host tissue (Figure 1). Given the key roles exerted by the microbiota and the Symbiodiniaceae in maintaining the host’s health and homeostasis [54,55,56], numerous studies have investigated the mechanisms by which these symbiotic partners can mitigate coral bleaching and increase resilience of the coral holobiont to other climate related stressors [36,57,58]. Transgenerational plasticity by conditioning maternal colonies before transmission and manipulating the horizontally acquired microorganisms has been proposed as a potential pathway to facilitate coral acclimatization and adaptation [99]

Symbiodiniaceae

The Microbiota

Bacteria

Viruses

Other Microbial Members

Coral Bleaching

Adaptive Dysbiosis without Symbiodiniaceae Community Restructuring

Findings

Microbiome Manipulations