School of BioSciences - Research Publications

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    Coral restoration and adaptation in Australia: The first five years
    McLeod, IM ; Hein, MY ; Babcock, R ; Bay, L ; Bourne, DG ; Cook, N ; Doropoulos, C ; Gibbs, M ; Harrison, P ; Lockie, S ; van Oppen, MJH ; Mattocks, N ; Page, CA ; Randall, CJ ; Smith, A ; Smith, HA ; Suggett, DJ ; Taylor, B ; Vella, KJ ; Wachenfeld, D ; Bostrom-Einarsson, L ; Guest, JR (PUBLIC LIBRARY SCIENCE, 2022-11-30)
    While coral reefs in Australia have historically been a showcase of conventional management informed by research, recent declines in coral cover have triggered efforts to innovate and integrate intervention and restoration actions into management frameworks. Here we outline the multi-faceted intervention approaches that have developed in Australia since 2017, from newly implemented in-water programs, research to enhance coral resilience and investigations into socio-economic perspectives on restoration goals. We describe in-water projects using coral gardening, substrate stabilisation, coral repositioning, macro-algae removal, and larval-based restoration techniques. Three areas of research focus are also presented to illustrate the breadth of Australian research on coral restoration, (1) the transdisciplinary Reef Restoration and Adaptation Program (RRAP), one of the world's largest research and development programs focused on coral reefs, (2) interventions to enhance coral performance under climate change, and (3) research into socio-cultural perspectives. Together, these projects and the recent research focus reflect an increasing urgency for action to confront the coral reef crisis, develop new and additional tools to manage coral reefs, and the consequent increase in funding opportunities and management appetite for implementation. The rapid progress in trialling and deploying coral restoration in Australia builds on decades of overseas experience, and advances in research and development are showing positive signs that coral restoration can be a valuable tool to improve resilience at local scales (i.e., high early survival rates across a variety of methods and coral species, strong community engagement with local stakeholders). RRAP is focused on creating interventions to help coral reefs at multiple scales, from micro scales (i.e., interventions targeting small areas within a specific reef site) to large scales (i.e., interventions targeting core ecosystem function and social-economic values at multiple select sites across the Great Barrier Reef) to resist, adapt to and recover from the impacts of climate change. None of these interventions aim to single-handedly restore the entirety of the Great Barrier Reef, nor do they negate the importance of urgent climate change mitigation action.
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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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    Advancing the protection of marine life through genomics
    van Oppen, MJH ; Coleman, MA ; Knowlton, N (PUBLIC LIBRARY SCIENCE, 2022-10)
    The rapid growth in genomic techniques provides the potential to transform how we protect, manage, and conserve marine life. Further, solutions to boost the resilience of marine species to climate change and other disturbances that characterize the Anthropocene require transformative approaches, made more effective if guided by genomic data. Although genetic techniques have been employed in marine conservation for decades and the availability of genomic data is rapidly expanding, widespread application still lags behind other data types. This Essay reviews how genetics and genomics have been utilized in management initiatives for ocean conservation and restoration, highlights success stories, and presents a pathway forward to enhance the uptake of genomic data for protecting our oceans.
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    The coral Acropora loripes genome reveals an alternative pathway for cysteine biosynthesis in animals
    Salazar, OR ; Arun, PN ; Cui, G ; Bay, LK ; Van Oppen, MJH ; Webster, NS ; Aranda, M (AMER ASSOC ADVANCEMENT SCIENCE, 2022-09-23)
    The metabolic capabilities of animals have been derived from well-studied model organisms and are generally considered to be well understood. In animals, cysteine is an important amino acid thought to be exclusively synthesized through the transsulfuration pathway. Corals of the genus Acropora have lost cystathionine β-synthase, a key enzyme of the transsulfuration pathway, and it was proposed that Acropora relies on the symbiosis with dinoflagellates of the family Symbiodiniaceae for the acquisition of cysteine. Here, we identify the existence of an alternative pathway for cysteine biosynthesis in animals through the analysis of the genome of the coral Acropora loripes. We demonstrate that these coral proteins are functional and synthesize cysteine in vivo, exhibiting previously unrecognized metabolic capabilities of animals. This pathway is also present in most animals but absent in mammals, arthropods, and nematodes, precisely the groups where most of the animal model organisms belong to, highlighting the risks of generalizing findings from model organisms.
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    A decade of coral biobanking science in Australia-transitioning into applied reef restoration
    Hobbs, RJ ; O'Brien, JK ; Bay, LK ; Severati, A ; Spindler, R ; Henley, EM ; Quigley, KM ; Randall, CJ ; van Oppen, MJH ; Carter, V ; Zuchowicz, N ; Hagedorn, M ; Daly, J (FRONTIERS MEDIA SA, 2022-09-16)
    Active restoration or intervention programs will be required in the future to support the resilience and adaptation of coral reef ecosystems in the face of climate change. Selective propagation of corals ex situ can help conserve keystone species and the ecosystems they underpin; cross-disciplinary research and communication between science and industry are essential to this success. Zoos and aquaria have a long history of managing ex situ breed-for-release programs and have led the establishment of wildlife biobanks (collections of cryopreserved living cells) along with the development of associated reproductive technologies for their application to wildlife conservation. Taronga Conservation Society Australia’s CryoDiversity Bank includes cryopreserved coral sperm from the Great Barrier Reef, which represents the largest repository from any reef system around the globe. This paper presents results from an inventory review of the current collection. The review highlighted the skew toward five Acropora species and the necessity to increase the taxonomic diversity of the collection. It also highlighted the need to increase geographic representation, even for the most well represented species. The inventory data will inform Taronga’s future research focus and sampling strategy to maximize genetic variation and biodiversity within the biobank and provide a test case for other practitioners implementing biobanking strategies for coral conservation around the world. Through co-investment and collaboration with research partners over the next decade, Taronga will prioritize and resource critical applied research and expand biobanking efforts to assist interventions for reef recovery and restoration.
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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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    Improved Cladocopium goreaui Genome Assembly Reveals Features of a Facultative Coral Symbiont and the Complex Evolutionary History of Dinoflagellate Genes
    Chen, Y ; Shah, S ; Dougan, KE ; van Oppen, MJH ; Bhattacharya, D ; Chan, CX (MDPI, 2022-08)
    Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35-36% have putatively originated via horizontal gene transfer (HGT), predominantly (19-23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10-11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.
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    Challenges of sperm cryopreservation in transferring heat adaptation of corals across ocean basins
    Howells, EJ ; Hagedorn, M ; Van Oppen, MJH ; Burt, JA (PEERJ INC, 2022-05-27)
    Reef-building corals live very close to their upper thermal limits and their persistence is imperiled by a rapidly warming climate. Human interventions may be used to increase the thermal limits of sensitive corals by cross-breeding with heat-adapted populations. However, the scope of breeding interventions is constrained by regional variation in the annual reproductive cycle of corals. Here we use cryopreservation technology to overcome this barrier and cross-breed conspecific coral populations across ocean basins for the first time. During regional spawning events, sperm samples were cryopreserved from populations of the widespread Indo-Pacific coral, Platygyra daedalea, from the southern Persian Gulf (maximum daily sea surface temperature of 36 °C), the Oman Sea (33 °C), and the central Great Barrier Reef (30 °C). These sperm samples were thawed during a later spawning event to test their ability to fertilize freshly spawned eggs of P. daedalea colonies from the central Great Barrier Reef. Average fertilization success for the Persian Gulf (9%) and Oman Sea (6%) sperm were 1.4-2.5 times lower than those for the native cryopreserved sperm from Great Barrier Reef (13-15%), potentially due to lower sperm quality of the Middle Eastern sperm and/or reproductive incompatibility between these distant populations. Overall, fertilization success with cryopreserved sperm was low compared with fresh sperm (>80%), likely due to the low motility of thawed sperm (≤5%, reduced from 50% to >90% in fresh sperm). To evaluate whether cross-bred offspring had enhanced thermal tolerance, the survival of larvae sired by Persian Gulf cryopreserved sperm, Great Barrier Reef cryopreserved sperm, and Great Barrier Reef fresh sperm was monitored for six days at ambient (27 °C) and elevated (33 °C) temperature. Against expectations of thermal tolerance enhancement, survival of larvae sired by Persian Gulf cryopreserved sperm was 2.6 times lower than larvae sired by Great Barrier Reef fresh sperm at 33 °C (27% versus 71%), but did not differ at 27 °C (77% versus 84%). This lack of enhanced thermal tolerance was unlikely due to outbreeding depression as survival was equally poor in larvae sired by Great Barrier Reef cryopreserved sperm. Rather, follow-up tests showed that cryoprotectant exposure during fertilization (0.1% DMSO) has a negative effect on the survival of P. daedalea larvae which is exacerbated at elevated temperature. Collectively, our findings highlight challenges of breeding corals for enhanced thermal tolerance using cryopreserved sperm, which may be overcome by methodological advances in the collection and preservation of high-quality motile sperm and minimizing the exposure time of eggs to cryoprotectants.
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    Fluorescence lifetime imaging microscopy (FLIM): a non-traditional approach to study host-microbial symbioses
    Deore, P ; Wanigasuriya, I ; Ching, SJTM ; Brumley, DR ; van Oppen, MJH ; Blackall, LL ; Hinde, E (CSIRO PUBLISHING, 2022)
    Corals and their photosynthetic endosymbiotic algae (Symbiodiniaceae) produce a strong autofluorescent signal that spans the visible to near-infrared (NIR) spectrum. However, this broad-spectrum emission hinders the use of fluorescence in situ hybridisation (FISH) for the study of bacterial heterogeneity within the different niches of corals and Symbiodiniaceae, because FISH fluorophores also fluoresce within the visible to NIR spectrum. A solution to this impediment is to use fluorescence lifetime imaging microscopy (FLIM). The ‘lifetime’ property of fluorophores is a feature that enables sample (e.g. coral/Symbiodiniaceae) autofluorescence to be distinguished from FISH-labelled bacteria. In this manner, the location of bacteria around and within Symbiodiniaceae can be quantified along with their identity and spatial distribution. Furthermore, the ‘lifetime’ of the host and associated microbe cellular autofluorescence can be analysed in terms of endogenous fluorophore composition (e.g. metabolic co-factors, aromatic amino acids) and serves as information for symbiotic versus parasitic host-microbe association.
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    Colonization and metabolite profiles of homologous, heterologous and experimentally evolved algal symbionts in the sea anemone Exaiptasia diaphana
    Ching, SJTM ; Chan, WY ; Perez-Gonzalez, A ; Hillyer, KE ; Buerger, P ; van Oppen, MJH (SPRINGERNATURE, 2022-03-30)
    The sea anemone, Exaiptasia diaphana, is a model of coral-dinoflagellate (Symbiodiniaceae) symbiosis. However, little is known of its potential to form symbiosis with Cladocopium-a key Indo-Pacific algal symbiont of scleractinian corals, nor the host nutritional consequences of such an association. Aposymbiotic anemones were inoculated with homologous algal symbionts, Breviolum minutum, and seven heterologous strains of Cladocopium C1acro (wild-type and heat-evolved) under ambient conditions. Despite lower initial algal cell density, Cladocopium C1acro-anemeones achieved similar cell densities as B. minutum-anemones by week 77. Wild-type and heat-evolved Cladocopium C1acro showed similar colonization patterns. Targeted LC-MS-based metabolomics revealed that almost all significantly different metabolites in the host and Symbiodiniaceae fractions were due to differences between Cladocopium C1acro and B. minutum, with little difference between heat-evolved and wild-type Cladocopium C1acro at week 9. The algal fraction of Cladocopium C1acro-anemones was enriched in metabolites related to nitrogen storage, while the host fraction of B. minutum-anemones was enriched in sugar-related metabolites. Compared to B. minutum, Cladocopium C1acro is likely slightly less nutritionally beneficial to the host under ambient conditions, but more capable of maintaining its own growth when host nitrogen supply is limited. Our findings demonstrate the value of E. diaphana to study experimentally evolved Cladocopium.