Defining Coral Bleaching as a Microbial Dysbiosis within the Coral Holobiont

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.

Keywords: Symbiodiniaceae; adaptive dysbiosis hypothesis; coral bleaching; holobiont; microbiota.

Figure 1

Coral bleaching. The upper photographs show a reef landscape (reef slope) before (a) and during (b) the massive bleaching event of 2016 at Moorea, French Polynesia. The bottom macro-photographs show a close-up lateral view of the polyps of the scleractinian coral Pocillopora damicornis experiencing bleaching: unbleached (healthy) polyps with visible Symbiodiniaceae (c), partially bleached polyps with low density of Symbiodiniaceae (d), and bleached polyps without Symbiodiniaceae and transparent tissue (e). Photographs are courtesy of Y. Chancerelle (a, b), and L. Hédouin (c–e) (CRIOBE, Moorea).

Figure 2

Coral microhabitats and their associated microorganisms. The diagram on the left illustrates a healthy coral (top) and a close-up transversal view of one polyp to illustrate the tissue layers (bottom). Diagrams on the right represent a close up of a cross-section of the coral tissues of a tentacle (a) and the basal part of the polyp (b), showing the distribution of the Symbiodiniaceae, bacteria, and cell-associated microbial aggregates (CAMAs) in the external environment, surface layer, ectodermis, gastrodermis, gastrovascular cavity, and skeleton. The size of the Symbiodiniaceae and microbes has been modified for illustration purposes. For an accurate size representation, see [90,91,92].

Figure 3

Holobiont dysbiosis phases associated with their coral bleaching states. The diagram illustrates an environmental stressor (increased temperature) inducing the disruption of the initial microbiome, leading to a dysbiosis state (stage 1) where the coral holobiont remains healthy (no sign of bleaching) despite the increase in the abundance of native opportunistic bacterial species and the settlement of invading pathogens and other opportunistic bacteria from the surrounding environment. The microbiota could act as a buffer and revert to its initial bacterial composition, representing an adaptive dysbiosis; or the environmental stressor could exceed the buffer capacity of the microbiota leading to another dysbiosis state (stage 2), where opportunistic bacteria and pathogens will slowly replace the initial microbiota, while the coral holobiont still remains healthy. Metagenomic plasticity, here referring to the addition of novel bacterial species and functions (but changes in relative abundances of native bacteria can also occur), either leads to another adaptive dysbiosis; or the environmental stressor exceeds once again the buffer capacity of the microbiota leading to another dysbiosis state (stage 3), where transient bleaching can be observed. Corals can revert to a healthy state by recovering a better suited Symbiodiniaceae assemblage, either by adjusting the relative abundance of native species from a low-background (shuffling), here referring to the increase in heat-tolerant Durusdinium species; or by recruiting exogenous species from the surrounding environment that are better adapted to elevated temperature (switching). If the stressor causes an abrupt change in the reef environment or persists for long periods, the adaptive dysbiosis will not act as a mechanism of environmental adaptation. In that case, the traumatic dysbiosis occurs with the permanent loss of the Symbiodiniaceae partners leading to coral death, and ultimately to a reef ecosystem dominated by algae and cyanobacteria (phase shifts). Each dotted circle represents the microbiome of a coral at each of the dysbiosis stages described, while the bar plots illustrate the declining number of “good microorganisms” and the increasing number of “bad” ones within the coral microbiome at each of the dysbiosis stages. The number and size of the Symbiodiniaceae and microbes within the coral tissues has been modified for illustration purposes.