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    Exploring microbiome engineering as a strategy for improved thermal tolerance in Exaiptasia diaphana
    Dungan, AM ; Hartman, LM ; Blackall, LL ; van Oppen, MJH (WILEY, 2022-02-19)
    AIMS: Fourteen percent of all living coral, equivalent to more than all the coral on the Great Barrier Reef, has died in the past decade as a result of climate change-driven bleaching. Inspired by the 'oxidative stress theory of coral bleaching', we investigated whether a bacterial consortium designed to scavenge free radicals could integrate into the host microbiome and improve thermal tolerance of the coral model, Exaiptasia diaphana. METHODS AND RESULTS: E. diaphana anemones were inoculated with a consortium of high free radical scavenging (FRS) bacteria, a consortium of congeneric low FRS bacteria, or sterile seawater as a control, then exposed to elevated temperature. Increases in the relative abundance of Labrenzia during the first 2 weeks following the last inoculation provided evidence for temporary inoculum integration into the E. diaphana microbiome. Initial uptake of other consortium members was inconsistent, and these bacteria did not persist either in E. diaphana's microbiome over time. Given their non-integration into the host microbiome, the ability of the FRS consortium to mitigate thermal stress could not be assessed. Importantly, there were no physiological impacts (negative or positive) of the bacterial inoculations on the holobiont. CONCLUSIONS: The introduced bacteria were not maintained in the anemone microbiome over time, thus, their protective effect is unknown. Achieving long-term integration of bacteria into cnidarian microbiomes remains a research priority. SIGNIFICANCE AND IMPACT OF THE STUDY: Microbiome engineering strategies to mitigate coral bleaching may assist coral reefs in their persistence until climate change has been curbed. This study provides insights that will inform microbiome manipulation approaches in coral bleaching mitigation research.
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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 Science and Business Media LLC, 2022-08-01)
    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 model Exaiptasia diaphana to exogenous antioxidants during thermal stress. Here, we replicate these experiments using E.diaphana with 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.diaphana exposed 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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    Development of a free radical scavenging bacterial consortium to mitigate oxidative stress in cnidarians
    Dungan, AM ; Bulach, D ; Lin, H ; van Oppen, MJH ; Blackall, LL (WILEY, 2021-07-14)
    Corals are colonized by symbiotic microorganisms that profoundly influence the animal's health. One noted symbiont is a single-celled alga (in the dinoflagellate family Symbiodiniaceae), which provides the coral with most of its fixed carbon. Thermal stress increases the production of reactive oxygen species (ROS) by Symbiodiniaceae during photosynthesis. ROS can both damage the algal symbiont's photosynthetic machinery and inhibit its repair, causing a positive feedback loop for the toxic accumulation of ROS. If not scavenged by the antioxidant network, excess ROS may trigger a signaling cascade ending with the coral host and algal symbiont disassociating in a process known as bleaching. We use Exaiptasia diaphana as a model for corals and constructed a consortium comprised of E. diaphana-associated bacteria capable of neutralizing ROS. We identified six strains with high free radical scavenging (FRS) ability belonging to the families Alteromonadaceae, Rhodobacteraceae, Flavobacteriaceae and Micrococcaceae. In parallel, we established a consortium of low FRS isolates consisting of genetically related strains. Bacterial whole genome sequences were used to identify key pathways that are known to influence ROS.
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    Short-Term Exposure to Sterile Seawater Reduces Bacterial Community Diversity in the Sea Anemone, Exaiptasia diaphana
    Dungan, AM ; van Oppen, MJH ; Blackall, LL (FRONTIERS MEDIA SA, 2021-01-21)
    The global decline of coral reefs heightens the need to understand how corals may persist under changing environmental conditions. Restructuring of the coral-associated bacterial community, either through natural or assisted strategies, has been suggested as a means of adaptation to climate change. A low complexity microbial system would facilitate testing the efficacy of microbial restructuring strategies. We used the model organism for corals, Exaiptasia diaphana, and determined that short-term (3 weeks) exposure to filter-sterilized seawater conditions alone reduced the complexity of the microbiome. Metabarcoding of the V5–V6 region of the bacterial 16S rRNA gene revealed that alpha diversity was approximately halved in anemones reared in filter-sterilized seawater compared to controls reared in unfiltered seawater and that the composition (beta diversity) differed significantly between the two. By reducing the complexity of the E. diaphana microbiome, the development of a system for testing assisted strategies such as probiotics, is more feasible.
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    Development of a free radical scavenging probiotic to mitigate coral bleaching
    Dungan, A ; Bulach, D ; Lin, H ; van Oppen, M ; Blackall, L (Cold Spring Harbor Laboratory, 2020-07-03)

    ABSTRACT

    Corals are colonized by symbiotic microorganisms that exert a profound influence on the animal’s health. One noted symbiont is a single-celled alga (from the family Symbiodiniaceae ), which provides the coral with most of its fixed carbon. During thermal stress, hyperactivity of photosynthesis results in a toxic accumulation of reactive oxygen species (ROS). If not scavenged by the antioxidant network, ROS may trigger a signaling cascade ending with the coral host and algal symbiont disassociating; this process is known as bleaching. Our goal was to construct a probiotic comprised of host-associated bacteria able to neutralize free radicals such as ROS. Using the coral model, the anemone Exaiptasia diaphana , and pure bacterial cultures isolated from the model animal, we identified six strains with high free radical scavenging ability belonging to the families Alteromonadaceae, Rhodobacteraceae, Flavobacteriaceae , and Micrococcaceae . In parallel, we established a “negative” probiotic consisting of genetically related strains with poor free radical scavenging capacities. From their whole genome sequences, we explored genes of interest that may contribute to their potential beneficial roles, which may help facilitate the therapeutic application of a bacterial probiotic. In particular, the occurrence of key pathways that are known to influence ROS in each of the strains has been inferred from the genomes sequences and are reported here.

    IMPORTANCE

    Coral bleaching is tightly linked to the production of reactive oxygen species (ROS), which accumulates to a toxic level in algae-harboring host cells leading to coral-algal dissociation. Interventions targeting ROS accumulation, such as the application of exogenous antioxidants, have shown promise for maintaining the coral-algal partnership. With the feasibility of administering antioxidants directly to corals being low, we aim to develop a probiotic to neutralize toxic ROS during a thermal stress event. This probiotic can be tested with corals or a coral model to assess its efficacy in improving coral resistance to environmental stress.
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    Exaiptasia diaphana from the great barrier reef: a valuable resource for coral symbiosis research
    Dungan, AM ; Hartman, LM ; Tortorelli, G ; Belderok, R ; Lamb, AM ; Pisan, L ; McFadden, GI ; Blackall, LL ; van Oppen, MJH (SPRINGER, 2020-02-06)
    The sea anemone, Exaiptasia diaphana, previously known as Exaiptasia pallida or Aiptasia pallida, has become increasingly popular as a model for cnidarian-microbiome symbiosis studies due to its relatively rapid growth, ability to reproduce sexually and asexually, and symbiosis with diverse prokaryotes and the same microalgal symbionts (family Symbiodiniaceae) as its coral relatives. Clonal E. diaphana strains from Hawaii, the Atlantic Ocean, and Red Sea are now established for use in research. Here, we introduce Great Barrier Reef (GBR)-sourced E. diaphana strains as additions to the model repertoire. Sequencing of the 18S rRNA gene confirmed the anemones to be E. diaphana while genome-wide single nucleotide polymorphism analysis revealed four distinct genotypes. Based on Exaiptasia-specific inter-simple sequence repeat (ISSR)-derived sequence characterized amplified region (SCAR) marker and gene loci data, these four E. diaphana genotypes are distributed across several divergent phylogenetic clades with no clear phylogeographical pattern. The GBR E. diaphana genotypes comprised three females and one male, which all host Breviolum minutum as their homologous Symbiodiniaceae endosymbiont. When acclimating to an increase in light levels from 12 to 28 μmol photons m−2 s−1, the genotypes exhibited significant variation in maximum quantum yield of Symbiodiniaceae photosystem II and Symbiodiniaceae cell density. The comparatively high levels of physiological and genetic variability among GBR anemone genotypes make these animals representative of global E. diaphana diversity and thus excellent model organisms. The addition of these GBR strains to the worldwide E. diaphana collection will contribute to cnidarian symbiosis research, particularly in relation to the climate resilience of coral reefs.