School of BioSciences

Coral reefs support a wide range of marine species and are crucial for our economy. However, current climate change and associated summer heatwaves cause reduced coral health and high mortality rates. An important aspect of coral reefs is a mutualism between the cnidarian host and endosymbiotic algae in the family Symbiodiniaceae, which provide more than 90 % of the coral energy through photosynthesis under the healthy mutualistic relationship. However, stressful environmental conditions such as elevated ocean temperature cause coral bleaching, which is the loss of Symbiodiniaceae from coral tissues. To increase the thermal tolerance of the corals, heat-evolved strains of the Symbiodiniaceae species Cladocopium C1acro were previously obtained through experimental evolution in vitro. Of the ten heat-evolved Symbiodiniaceae strains, three strains confer enhanced bleaching tolerance to Acropora tenuis coral larvae. To test whether these strains improve the thermal tolerance of another host species, I exposed sea anemones, Exaiptasia diaphana, inoculated with each of eight strains of Symbiodiniaceae (the homologous symbiont, Breviolum minutum; the wild-type and six heat-evolved strains of Cladocopium C1acro) to elevated temperature. My findings showed that the thermal tolerance of E. diaphana varied depending on the inoculated Symbiodiniaceae strains, however, the thermal tolerance ranking differed from that observed in the previous coral larval experiment. Metabolomics analysis of the host fraction indicated that the translocation of sugar was significantly lower under the elevated temperature treatment for all host-symbiont pairs, which supports one of the bleaching hypotheses that coral bleaching is caused Symbiodiniaceae becoming parasitic under elevated temperature. This study revealed important insight into the cnidarian-Symbiodiniaceae interaction under elevated temperature and provided an insight into the coral bleaching hypothesis.

The coral holobiont is a complex metaorganism where the coral polyps, microeukaryotes, prokaryotes and viruses interact within the three-dimensional structure of the coral colony. These interactions have shaped corals over a period spanning 400 million years - when Scleractinians began diversifying in the Palaeozoic - facilitating the success of these animals in tropical, temperate and arctic environments as well shallow and deep oceans. Corals strongly rely on their microbial partners, for instance, the relationship with unicellular algae in the family Symbiodiniaceae is an emblematic example of host-symbiont nutritional exchanges, but more recently other functions like antimicrobial activity, bioactive compounds synthesis and thermal tolerance have been attributed to members of the holobiont. The microbiota harboured in the coral skeleton, referred to as the endolithic microbiome, is an often-overlooked component of this system. These endoliths colonize coral nubbins just a few days after the settlement and they are thought to be involved in several biochemical pathways of the holobiont. Among them are the endolithic algae, mainly represented by the genus Ostreobium. These photosynthetic microeukaryotes are keystone species in the skeletal environment, where they modify the physical ultrastructure by means of their boring action, shape the physicochemical gradients through their autotrophic metabolism and ultimately influence the presence and abundance of other holobiont members. Endolithic algae have also attracted attention because of their potential ability to transfer sugars to the host, a process that can aid coral survival during bleaching events when the symbiosis with the microalgae populating the tissue gets impaired. In recent times the studies investigating coral holobionts have risen but observations on broader scales are still scarce and this is what this thesis is about. Currently our knowledge of the coral skeleton and its microbiota is still limited with few studies focused on understanding the diversity and function of this endolithic community, therefore in Chapter 2 I brought it together and reviewed the roles that endoliths play in the coral holobiont, which include shaping the coral physicochemical gradients, nutritional exchanges and decalcification of the skeletal matrix. Here, I proposed that the metabolism of the microbial community shapes the physicochemical microniches of the coral skeleton that, along with other processes like priority effects and dispersal limitation define the microbial community assembly. In Chapter 3 I used multiple techniques to characterize the endolithic microbiome of one of the most common corals found in the Great Barrier Reef, Isopora palifera. Here, in contrast to a previous study on the same coral species, I showed that oxygenic phototrophs were the dominant functional group. In Chapter 4 I employed a rigorous experimental design, molecular characterization of the microbiota and innovative techniques including micro-CT scanning to quantify the contribution of host evolutionary history, skeletal architecture and reproductive mode on the bacterial community composition of tissue and skeleton. Variation partitioning analysis showed that these predictors explained 14% of the tissue and 13% of the skeletal microbiome composition and influenced the presence and abundance of key coral-bacterial symbiosis. A large fraction of bacteria was present both the coral tissue and skeleton but their abundance in the two compartments differed, supporting the hypothesis that the coral skeleton can function as a microbial reservoir to the rest of the holobiont. Additionally, I found that coral tissue and skeleton bacterial communities were dominated by rare bacteria, and the groups Cyclobacteriaceae, Paramaledivibacter and Roseospira were persistently associated with corals but are either new to the coral microbiome field or understudied. In Chapter 4 I linked the physicochemical environment of the coral skeleton to the colonizing microbiome. The coral skeleton can be seen as a microbial environment where its biotic and abiotic components interact and influence each other. I used two coral species with pronounced differences in their skeletal architecture, Porites lutea and Paragoniastrea australensis, and I showed that their skeletons are characterized by steep physicochemical gradients shaped by the metabolism of the microbial community, which is in turn influenced by these gradients. Canonical correspondence analysis showed statistically meaningful correlations between bacterial ASVs and O2 and pH gradients suggesting that the presence and relative abundance of bacteria affiliated to Chlorobi, Spirochaeta and Alteromonas were influenced by the physicochemical environment. Additionally, by using hyperspectral reflectance imaging and molecular characterization of the microbiome I showed that corals harbour a wide diversity of phototrophs and that different coral species have similar communities but with very different spatial organizations. This thesis describes the microbial communities living in associations with several corals species and contributes to unraveling those abiotic and biotic processes driving the coral holobiont structure. Here I highlight the variability of the microbiome across coral species, between anatomical compartments (tissue and skeleton) and across different layers of the coral skeleton. My data show that the physicochemical environment of the coral skeleton is dynamic and shaped by the interaction between the metabolism of the microbial community harbored within it and the characteristic skeletal architecture of each coral species. Furthermore, based on my results, I propose that the endolithic community interacts with the tissue microbiome as well as with the host suggesting that the coral skeleton is an integral part of the coral holobiont.

School of BioSciences - Theses

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