School of BioSciences - Research Publications

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    A role for bacterial experimental evolution in coral bleaching mitigation?
    Maire, J ; van Oppen, MJH (CELL PRESS, 2022-03)
    Coral reefs are rapidly declining because of widespread mass coral bleaching causing extensive coral mortality. Elevated seawater temperatures are the main drivers of coral bleaching, and climate change is increasing the frequency and severity of destructive marine heatwaves. Efforts to enhance coral thermal bleaching tolerance can be targeted at the coral host or at coral-associated microorganisms (e.g., dinoflagellate endosymbionts and bacteria). The literature on experimental evolution of bacteria suggests that it has value as a tool to increase coral climate resilience. We provide a workflow on how to experimentally evolve coral-associated bacteria to confer thermal tolerance to coral hosts and emphasize the value of implementing this approach in coral reef conservation and restoration efforts.
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    Effects of Ocean Warming on the Underexplored Members of the Coral Microbiome
    Maire, J ; Buerger, P ; Chan, WY ; Deore, P ; Dungan, AM ; Nitschke, MR ; van Oppen, MJH (OXFORD UNIV PRESS INC, 2022-12-30)
    The climate crisis is one of the most significant threats to marine ecosystems. It is leading to severe increases in sea surface temperatures and in the frequency and magnitude of marine heatwaves. These changing conditions are directly impacting coral reef ecosystems, which are among the most biodiverse ecosystems on Earth. Coral-associated symbionts are particularly affected because summer heatwaves cause coral bleaching-the loss of endosymbiotic microalgae (Symbiodiniaceae) from coral tissues, leading to coral starvation and death. Coral-associated Symbiodiniaceae and bacteria have been extensively studied in the context of climate change, especially in terms of community diversity and dynamics. However, data on other microorganisms and their response to climate change are scarce. Here, we review current knowledge on how increasing temperatures affect understudied coral-associated microorganisms such as archaea, fungi, viruses, and protists other than Symbiodiniaceae, as well as microbe-microbe interactions. We show that the coral-microbe symbiosis equilibrium is at risk under current and predicted future climate change and argue that coral reef conservation initiatives should include microbe-focused approaches.
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    Long-Term Heat Selection of the Coral Endosymbiont Cladocopium C1acro (Symbiodiniaceae) Stabilizes Associated Bacterial Communities
    Buerger, P ; Vanstone, RT ; Maire, J ; van Oppen, MJH (MDPI, 2022-05)
    Heat-tolerant strains of the coral endosymbiont, Cladocopium C1acro (Symbiodiniaceae), have previously been developed via experimental evolution. Here, we examine physiological responses and bacterial community composition (using 16S rRNA gene metabarcoding) in cultures of 10 heat-evolved (SS) and 9 wild-type (WT) strains, which had been exposed for 6 years to 31 °C and 27 °C, respectively. We also examine whether the associated bacterial communities were affected by a three-week reciprocal transplantation to both temperatures. The SS strains had bacterial communities with lower diversities that showed more stability and lower variability when exposed to elevated temperatures compared with the WT strains. Amplicon sequence variants (ASVs) of the bacterial genera Labrenzia, Algiphilus, Hyphobacterium and Roseitalea were significantly more associated with the SS strains compared with the WT strains. WT strains showed higher abundance of ASVs assigned to the genera Fabibacter and Tropicimonas. We hypothesize that these compositional differences in associated bacterial communities between SS and WT strains also contribute to the thermal tolerance of the microalgae. Future research should explore functional potential between bacterial communities using metagenomics to unravel specific genomic adaptations.
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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 Bacterial Symbionts in Corals: Challenges and Future Directions
    Maire, J ; Blackall, LL ; van Oppen, MJH (MDPI, 2021-11)
    Corals are the main primary producers of coral reefs and build the three-dimensional reef structure that provides habitat to more than 25% of all marine eukaryotes. They harbor a complex consortium of microorganisms, including bacteria, archaea, fungi, viruses, and protists, which they rely on for their survival. The symbiosis between corals and bacteria is poorly studied, and their symbiotic relationships with intracellular bacteria are only just beginning to be acknowledged. In this review, we emphasize the importance of characterizing intracellular bacteria associated with corals and explore how successful approaches used to study such microorganisms in other systems could be adapted for research on corals. We propose a framework for the description, identification, and functional characterization of coral-associated intracellular bacterial symbionts. Finally, we highlight the possible value of intracellular bacteria in microbiome manipulation and mitigating coral bleaching.
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    Microbiome characterization of defensive tissues in the model anemone Exaiptasia diaphana
    Maire, J ; Blackall, LL ; van Oppen, MJH (BMC, 2021-05-21)
    BACKGROUND: Coral reefs are among the most diverse and productive ecosystems on Earth. This success relies on the coral's association with a wide range of microorganisms, including dinoflagellates of the family Symbiodiniaceae that provide coral hosts with most of their organic carbon requirements. While bacterial associates have long been overlooked, research on these microorganisms is gaining traction, and deciphering bacterial identity and function is greatly enhancing our understanding of cnidarian biology. Here, we investigated bacterial communities in defensive tissues (acontia) of the coral model, the sea anemone Exaiptasia diaphana. Acontia are internal filaments that are ejected upon detection of an external threat and release toxins to repel predators. RESULTS: Using culturing techniques and 16S rRNA gene metabarcoding we identified bacterial communities associated with acontia of four Great Barrier Reef-sourced E. diaphana genotypes. We show that bacterial communities are similar across genotypes, and dominated by Alteromonadaceae, Vibrionaceae, Rhodobacteraceae, and Saprospiraceae. By analyzing abundant amplicon sequence variants (ASVs) from metabarcoding data from acontia and comparing these to data from whole anemones, we identified five potentially important bacterial genera of the acontia microbiome: Vibrio, Sulfitobacter, Marivita, Alteromonas, and Lewinella. The role of these bacteria within the acontia remains uninvestigated but could entail assistance in defense processes such as toxin production. CONCLUSIONS: This study provides insight into potential bacterial involvement in cnidarian defense tissues and highlights the need to study bacterial communities in individual compartments within a holobiont.
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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.