School of BioSciences - Research Publications

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    Inoculation with Roseovarius increases thermal tolerance of the coral photosymbiont, Breviolum minutum
    Heric, K ; Maire, J ; Deore, P ; Perez-Gonzalez, A ; van Oppen, MJH (FRONTIERS MEDIA SA, 2023-08-10)
    Coral reefs are diverse marine ecosystems that have tremendous ecological and cultural value and support more than 25% of eukaryote marine biodiversity. Increased ocean temperatures and light intensity trigger coral bleaching, the breakdown of the relationship between corals and their photosymbionts, dinoflagellates of the family Symbiodiniaceae. This leaves corals without their primary energy source, thereby leading to starvation and, often, death. Coral bleaching is hypothesized to occur due to an overproduction of reactive oxygen species (ROS) by Symbiodiniaceae, which subsequently accumulate in coral tissues. Bacterial probiotics have been proposed as an approach to mitigate coral bleaching, by reducing ROS levels in the coral holobiont through bacterial antioxidant production. Both corals and Symbiodiniaceae are known to associate with bacteria. However, the Symbiodiniaceae-bacteria relationship, and its impact on Symbiodiniaceae thermal tolerance, remains a poorly studied area. In this study, cultured Symbiodiniaceae of the species Breviolum minutum were treated with antibiotics to reduce their bacterial load. The cultures were subsequently inoculated with bacterial isolates from the genus Roseovarius that were isolated from the same B. minutum culture and showed either high or low ROS-scavenging abilities. The B. minutum cultures were then exposed to experimental heat stress for 16 days, and their health was monitored through measurements of cell density and photochemical efficiency of photosystem II. It was found that B. minutum inoculated with Roseovarius with higher ROS-scavenging abilities showed greater cell growth at elevated temperatures, compared to cultures inoculated with a Roseovarius strain with lower ROS-scavenging abilities. This suggests that Roseovarius may play a role in Symbiodiniaceae fitness at elevated temperatures. Analysis of Symbiodiniaceae-associated bacterial communities through 16S rRNA gene metabarcoding revealed that Roseovarius relative abundance increased in B. minutum cultures following inoculation and with elevated temperature exposure, highlighting the contribution they may have in shielding B. minutum from thermal stress, although other bacterial community changes may have also contributed to these observations. This study begins to unpick the relationship between Symbiodiniaceae and their bacteria and opens the door for the use of Symbiodiniaceae-associated bacteria in coral reef conservation approaches.
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    Assessing the contribution of bacteria to the heat tolerance of experimentally evolved coral photosymbionts
    Maire, J ; Deore, P ; Jameson, VJ ; Sakkas, M ; Perez-Gonzalez, A ; Blackall, LL ; van Oppen, MJH (WILEY, 2023-12)
    Coral reefs are extremely vulnerable to ocean warming, which triggers coral bleaching-the loss of endosymbiotic microalgae (Symbiodiniaceae) from coral tissues, often leading to death. To enhance coral climate resilience, the symbiont, Cladocopium proliferum was experimentally evolved for >10 years under elevated temperatures resulting in increased heat tolerance. Bacterial 16S rRNA gene metabarcoding showed the composition of intra- and extracellular bacterial communities of heat-evolved strains was significantly different from that of wild-type strains, suggesting bacteria responded to elevated temperatures, and may even play a role in C. proliferum thermal tolerance. To assess whether microbiome transplantation could enhance heat tolerance of the sensitive wild-type C. proliferum, we transplanted bacterial communities from heat-evolved to the wild-type strain and subjected it to acute heat stress. Microbiome transplantation resulted in the incorporation of only 30 low-abundance strains into the microbiome of wild-type cultures, while the relative abundance of 14 pre-existing strains doubled in inoculated versus uninoculated samples. Inoculation with either wild-type or heat-evolved bacterial communities boosted C. proliferum growth, although no difference in heat tolerance was observed between the two inoculation treatments. This study provides evidence that Symbiodiniaceae-associated bacterial communities respond to heat selection and may contribute to coral adaptation to climate change.
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    Comparing the Role of ROS and RNS in the Thermal Stress Response of Two Cnidarian Models, Exaiptasia diaphana and Galaxea fascicularis
    Doering, T ; Maire, J ; Chan, WY ; Perez-Gonzalez, A ; Meyers, L ; Sakamoto, R ; Buthgamuwa, I ; Blackall, LL ; van Oppen, MJH (MDPI, 2023-05-06)
    Coral reefs are threatened by climate change, because it causes increasingly frequent and severe summer heatwaves, resulting in mass coral bleaching and mortality. Coral bleaching is believed to be driven by an excess production of reactive oxygen (ROS) and nitrogen species (RNS), yet their relative roles during thermal stress remain understudied. Here, we measured ROS and RNS net production, as well as activities of key enzymes involved in ROS scavenging (superoxide dismutase and catalase) and RNS synthesis (nitric oxide synthase) and linked these metrics to physiological measurements of cnidarian holobiont health during thermal stress. We did this for both an established cnidarian model, the sea anemone Exaiptasia diaphana, and an emerging scleractinian model, the coral Galaxea fascicularis, both from the Great Barrier Reef (GBR). Increased ROS production was observed during thermal stress in both species, but it was more apparent in G. fascicularis, which also showed higher levels of physiological stress. RNS did not change in thermally stressed G. fascicularis and decreased in E. diaphana. Our findings in combination with variable ROS levels in previous studies on GBR-sourced E. diaphana suggest G. fascicularis is a more suitable model to study the cellular mechanisms of coral bleaching.
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    Lack of evidence for the oxidative stress theory of bleaching in the sea anemone, Exaiptasia diaphana, under elevated temperature
    Dungan, AM ; Maire, J ; Perez-Gonzalez, A ; Blackall, LL ; van Oppen, MJH (SPRINGER, 2022-08)
    Abstract To survive in nutrient-poor waters corals rely on a symbiotic association with intracellular microalgae. However, increased sea temperatures cause algal loss—known as coral bleaching—often followed by coral death. Some of the most compelling evidence in support of the ‘oxidative stress theory of coral bleaching’ comes from studies that exposed corals, cultures of their algal endosymbionts, or the coral modelExaiptasia diaphanato exogenous antioxidants during thermal stress. Here, we replicate these experiments usingE.diaphanawith the addition of the antioxidants ascorbate + catalase, catechin, or mannitol under ambient and elevated temperatures along with an antioxidant-free control. In the absence of exogenous antioxidants,E.diaphanaexposed to elevated temperatures bleached with no change in reactive oxygen species (ROS) levels associated with their microalgal cells. Ascorbate + catalase and mannitol treatments rescued the anemones from bleaching, although microalgal ROS levels increased in these antioxidant treatments under elevated temperature conditions. While bleaching was not associated with changes in net ROS for the intracellular algal symbionts, it is evident from our findings that excess ROS is connected to the bleaching phenotype as exogenous antioxidants were successful in mitigating the effects of thermal stress in cnidarians. This understanding may assist applied research that aims to reduce the impact of climate change on coral reefs.
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    Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs
    Maire, J ; Girvan, SK ; Barkla, SE ; Perez-Gonzalez, A ; Suggett, DJ ; Blackall, LL ; van Oppen, MJH (SPRINGERNATURE, 2021-07)
    Corals house a variety of microorganisms which they depend on for their survival, including endosymbiotic dinoflagellates (Symbiodiniaceae) and bacteria. While cnidarian-microorganism interactions are widely studied, Symbiodiniaceae-bacteria interactions are only just beginning to receive attention. Here, we describe the localization and composition of the bacterial communities associated with cultures of 11 Symbiodiniaceae strains from nine species and six genera. Three-dimensional confocal laser scanning and electron microscopy revealed bacteria are present inside the Symbiodiniaceae cells as well as closely associated with their external cell surface. Bacterial pure cultures and 16S rRNA gene metabarcoding from Symbiodiniaceae cultures highlighted distinct and highly diverse bacterial communities occur intracellularly, closely associated with the Symbiodiniaceae outer cell surface and loosely associated (i.e., in the surrounding culture media). The intracellular bacteria are highly conserved across Symbiodiniaceae species, suggesting they may be involved in Symbiodiniaceae physiology. Our findings provide unique new insights into the biology of Symbiodiniaceae.