Symbiodiniaceae‐bacteria interactions: rethinking metabolite exchange in reef‐building corals as multi‐partner metabolic networks

Abstract

Summary The intimate relationship between scleractinian corals and their associated microorganisms is fundamental to healthy coral reef ecosystems. Coral‐associated microbes (Symbiodiniaceae and other protists, bacteria, archaea, fungi and viruses) support coral health and resilience through metabolite transfer, inter‐partner signalling, and genetic exchange. However, much of our understanding of the coral holobiont relationship has come from studies that have investigated either coral‐Symbiodiniaceae or coral‐bacteria interactions in isolation, while relatively little research has focused on other ecological and metabolic interactions potentially occurring within the coral multi‐partner symbiotic network. Recent evidences of intimate coupling between phytoplankton and bacteria have demonstrated that obligate resource exchange between partners fundamentally drives their ecological success. Here, we posit that similar associations with bacterial consortia regulate Symbiodiniaceae productivity and are in turn central to the health of corals. Indeed, we propose that this bacteria‐Symbiodiniaceae‐coral relationship underpins the coral holobiont's nutrition, stress tolerance and potentially influences the future survival of coral reef ecosystems under changing environmental conditions. Resolving Symbiodiniaceae‐bacteria associations is therefore a logical next step towards understanding the complex multi‐partner interactions occurring in the coral holobiont.

Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching

“…Coral microbiota in a balanced status plays indispensable roles in holobiont health and contributes importantly to nutrient acquisition and the regulation of matter cycling (Rosenberg et al ., ; Bourne et al ., ; Bosch and McFall‐Ngai, ). Changing bacterial community composition may affect coral physiological status and increase the susceptibility to pathogens (Kushmaro et al ., , ; Koren and Rosenberg, ; Matthews et al ., ). Displacement of primary resident by other microorganisms, or shifts in the abundance of related members, has been linked with the appearance of bleaching or other symptoms (Cardenas et al ., ; Vezzulli et al ., ; Roder et al ., ).…”

“…They reportedly also contribute to bacterial and bacteria–host interactions (Thompson et al . ; Papenfort and Bassler ; Zhou et al ., ; Matthews et al ., ).…”

“…Blackstone and Golladay () and Matthews et al . () further pointed out that understanding the interactions between coral hosts and the multitude of symbiotic microorganisms is of critical importance for predicting the ability of corals to adapt and evolve in response to environmental change.…”

The Complexity of the Holobiont in the Red Sea Coral Euphyllia paradivisa under Heat Stress

“…Recent studies have presented evidence suggesting a new perspective on the cnidarian holobiont, where Symbiodiniaceae-bacterial interactions play a key role in the holobiont nutrient cycling, symbiont stability, and overall fitness (recently reviewed by [24]). The metabolic capabilities of the symbiotic bacteria, and their localization within and around the algal symbionts, support this hypothesis [17].…”

Development of a free radical scavenging probiotic to mitigate coral bleaching

“…Genomic evidence suggests that Symbiodiniaceae may have lost the capacity to synthesize vitamin B12 due to changes in their metabolic enzymes during their evolution[78], agreeing with other work that free-living Symbiodiniaceae depend on bacterial symbionts to gain access to this important cofactor[79]. The genes involved in the biosynthesis of vitamin B12 have been found in coral-associated bacteria, specifically L. aggregata cultured from the Caribbean coral, Orbicella faveolata[80].From the annotated draft genome sequence, using the cobP gene[77] as the genotypic indicator, both L. aggregata isolates are capable of Vitamin B12 biosynthesis.…”