School of BioSciences - Research Publications

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    Diversity and stability of coral endolithic microbial communities at a naturally high pCO(2) reef
    Marcelino, VR ; Morrow, KM ; van Oppen, MJH ; Bourne, DG ; Verbruggen, H (WILEY, 2017-10-01)
    The health and functioning of reef-building corals is dependent on a balanced association with prokaryotic and eukaryotic microbes. The coral skeleton harbours numerous endolithic microbes, but their diversity, ecological roles and responses to environmental stress, including ocean acidification (OA), are not well characterized. This study tests whether pH affects the diversity and structure of prokaryotic and eukaryotic algal communities associated with skeletons of Porites spp. using targeted amplicon (16S rRNA gene, UPA and tufA) sequencing. We found that the composition of endolithic communities in the massive coral Porites spp. inhabiting a naturally high pCO2 reef (avg. pCO2 811 μatm) is not significantly different from corals inhabiting reference sites (avg. pCO2 357 μatm), suggesting that these microbiomes are less disturbed by OA than previously thought. Possible explanations may be that the endolithic microhabitat is highly homeostatic or that the endolithic micro-organisms are well adapted to a wide pH range. Some of the microbial taxa identified include nitrogen-fixing bacteria (Rhizobiales and cyanobacteria), algicidal bacteria in the phylum Bacteroidetes, symbiotic bacteria in the family Endozoicomoniaceae, and endolithic green algae, considered the major microbial agent of reef bioerosion. Additionally, we test whether host species has an effect on the endolithic community structure. We show that the endolithic community of massive Porites spp. is substantially different and more diverse than that found in skeletons of the branching species Seriatopora hystrix and Pocillopora damicornis. This study reveals highly diverse and structured microbial communities in Porites spp. skeletons that are possibly resilient to OA.
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    Shifting paradigms in restoration of the world's coral reefs
    Van Oppen, MJH ; Gates, RD ; Blackall, LL ; Cantin, N ; Chakravarti, LJ ; Chan, WY ; Cormick, C ; Crean, A ; Damjanovic, K ; Epstein, H ; Harrison, PL ; Jones, TA ; Miller, M ; Pears, RJ ; Peplow, LM ; Raftos, DA ; Schaffelke, B ; Stewart, K ; Torda, G ; Wachenfeld, D ; Weeks, AR ; Putnam, HM (Wiley, 2017-09-01)
    Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine‐protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014–2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.
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    Expanding the Symbiodinium (Dinophyceae, Suessiales) Toolkit Through Protoplast Technology
    Levin, RA ; Suggett, DJ ; Nitschke, MR ; van Oppen, MJH ; Steinberg, PD (WILEY, 2017-09-01)
    Dinoflagellates within the genus Symbiodinium are photosymbionts of many tropical reef invertebrates, including corals, making them central to the health of coral reefs. Symbiodinium have therefore gained significant research attention, though studies have been constrained by technical limitations. In particular, the generation of viable cells with their cell walls removed (termed protoplasts) has enabled a wide range of experimental techniques for bacteria, fungi, plants, and algae such as ultrastructure studies, virus infection studies, patch clamping, genetic transformation, and protoplast fusion. However, previous studies have struggled to remove the cell walls from armored dinoflagellates, potentially due to the internal placement of their cell walls. Here, we produce the first Symbiodinium protoplasts from three genetically and physiologically distinct strains via incubation with cellulase and osmotic agents. Digestion of the cell walls was verified by a lack of Calcofluor White fluorescence signal and by cell swelling in hypotonic culture medium. Fused protoplasts were also observed, motivating future investigation into intra- and inter-specific somatic hybridization of Symbiodinium. Following digestion and transfer to regeneration medium, protoplasts remained photosynthetically active, regrew cell walls, regained motility, and entered exponential growth. Generation of Symbiodinium protoplasts opens exciting, new avenues for researching these crucial symbiotic dinoflagellates, including genetic modification.
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    Microsatellite allele sizes alone are insufficient to delineate species boundaries in Symbiodinium
    Howells, EJ ; Willis, BL ; Bay, LK ; Van Oppen, MJH (WILEY, 2016-06-01)
    Symbiodinium are a diverse group of unicellular dinoflagellates that are important nutritional symbionts of reef-building corals. Symbiodinium putative species ('types') are commonly identified with genetic markers, mostly nuclear and chloroplast encoded ribosomal DNA regions. Population genetic analyses using microsatellite loci have provided insights into Symbiodinium biogeography, connectivity and phenotypic plasticity, but are complicated by: (i) a lack of consensus criteria used to delineate inter- vs. intragenomic variation within species; and (ii) the high density of Symbiodinium in host tissues, which results in single samples comprising thousands of individuals. To address this problem, Wham & LaJeunesse (2016) present a method for identifying cryptic Symbiodinium species from microsatellite data based on correlations between allele size distributions and nongeographic genetic structure. Multilocus genotypes that potentially do not recombine in sympatry are interpreted as secondary 'species' to be discarded from downstream population genetic analyses. However, Symbiodinium species delineations should ideally incorporate multiple physiological, ecological and molecular criteria. This is because recombination tests may be a poor indicator of species boundaries in Symbiodinium due to their predominantly asexual mode of reproduction. Furthermore, discontinuous microsatellite allele sizes in sympatry may be explained by secondary contact between previously isolated populations and by mutations that occur in a nonstepwise manner. Limitations of using microsatellites alone to delineate species are highlighted in earlier studies that demonstrate occasional bimodal distributions of allele sizes within Symbiodinium species and considerable allele size sharing among Symbiodinium species. We outline these issues and discuss the validity of reinterpretations of our previously published microsatellite data from Symbiodinium populations on the Great Barrier Reef (Howells et al. 2013).
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    Congruent patterns of connectivity can inform management for broadcast spawning corals on the Great Barrier Reef
    Lukoschek, V ; Riginos, C ; van Oppen, MJH (WILEY, 2016-07-01)
    Connectivity underpins the persistence and recovery of marine ecosystems. The Great Barrier Reef (GBR) is the world's largest coral reef ecosystem and managed by an extensive network of no-take zones; however, information about connectivity was not available to optimize the network's configuration. We use multivariate analyses, Bayesian clustering algorithms and assignment tests of the largest population genetic data set for any organism on the GBR to date (Acropora tenuis, >2500 colonies; >50 reefs, genotyped for ten microsatellite loci) to demonstrate highly congruent patterns of connectivity between this common broadcast spawning reef-building coral and its congener Acropora millepora (~950 colonies; 20 reefs, genotyped for 12 microsatellite loci). For both species, there is a genetic divide at around 19°S latitude, most probably reflecting allopatric differentiation during the Pleistocene. GBR reefs north of 19°S are essentially panmictic whereas southern reefs are genetically distinct with higher levels of genetic diversity and population structure, most notably genetic subdivision between inshore and offshore reefs south of 19°S. These broadly congruent patterns of higher genetic diversities found on southern GBR reefs most likely represent the accumulation of alleles via the southward flowing East Australia Current. In addition, signatures of genetic admixture between the Coral Sea and outer-shelf reefs in the northern, central and southern GBR provide evidence of recent gene flow. Our connectivity results are consistent with predictions from recently published larval dispersal models for broadcast spawning corals on the GBR, thereby providing robust connectivity information about the dominant reef-building genus Acropora for coral reef managers.
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    Sperm dispersal distances estimated by parentage analysis in a brooding scleractinian coral
    Warner, PA ; Willis, BL ; van Oppen, MJH (WILEY, 2016-03-01)
    Within populations of brooding sessile corals, sperm dispersal constitutes the mechanism by which gametes interact and mating occurs, and forms the first link in the network of processes that determine specieswide connectivity patterns. However, almost nothing is known about sperm dispersal for any internally fertilizing coral. In this study, we conducted a parentage analysis on coral larvae collected from an area of mapped colonies, to measure the distance sperm disperses for the first time in a reef-building coral and estimated the mating system characteristics of a recently identified putative cryptic species within the Seriatopora hystrix complex (ShA; Warner et al. 2015). We defined consensus criteria among several replicated methods (COLONY 2.0, CERVUS 3.0, MLTR v3.2) to maximize accuracy in paternity assignments. Thirteen progeny arrays indicated that this putative species produces exclusively sexually derived, primarily outcrossed larvae (mean t(m) = 0.999) in multiple paternity broods (mean r(p) = 0.119). Self-fertilization was directly detected at low frequency for all broods combined (2.8%), but comprised 23% of matings in one brood. Although over 82% of mating occurred between colonies within 10 m of each other (mean sperm dispersal = 5.5 m ± 4.37 SD), we found no evidence of inbreeding in the established population. Restricted dispersal of sperm compared to slightly greater larval dispersal appears to limit inbreeding among close relatives in this cryptic species. Our findings establish a good basis for further work on sperm dispersal in brooding corals and provide the first information about the mating system of a newly identified and abundant cryptic species.
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    Microbiome engineering: enhancing climate resilience in corals
    Epstein, HE ; Smith, HA ; Torda, G ; van Oppen, MJH (WILEY, 2019-03-01)
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    Novel T4 bacteriophages associated with black band disease in corals
    Buerger, P ; Weynberg, KD ; Wood-Charlson, EM ; Sato, Y ; Willis, BL ; van Oppen, MJH (WILEY, 2019-06-01)
    Research into causative agents underlying coral disease have focused primarily on bacteria, whereas potential roles of viruses have been largely unaddressed. Bacteriophages may contribute to diseases through the lysogenic introduction of virulence genes into bacteria, or prevent diseases through lysis of bacterial pathogens. To identify candidate phages that may influence the pathogenicity of black band disease (BBD), communities of bacteria (16S rRNA) and T4-bacteriophages (gp23) were simultaneously profiled with amplicon sequencing among BBD-lesions and healthy-coral-tissue of Montipora hispida, as well as seawater (study site: the central Great Barrier Reef). Bacterial community compositions were distinct among BBD-lesions, healthy coral tissue and seawater samples, as observed in previous studies. Surprisingly, however, viral beta diversities based on both operational taxonomic unit (OTU)-compositions and overall viral community compositions of assigned taxa did not differ statistically between the BBD-lesions and healthy coral tissue. Nonetheless, relative abundances of three bacteriophage OTUs, affiliated to Cyanophage PRSM6 and Prochlorococcus phages P-SSM2, were significantly higher in BBD-lesions than in healthy tissue. These OTUs associated with BBD samples suggest the presence of bacteriophages that infect members of the cyanobacteria-dominated BBD community, and thus have potential roles in BBD pathogenicity.
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    Adaptation to reef habitats through selection on the coral animal and its associated microbiome
    van Oppen, MJH ; Bongaerts, P ; Frade, P ; Peplow, L ; Boyd, SE ; Nim, HT ; Bay, LK (WILEY, 2018-07-01)
    Spatially adjacent habitats on coral reefs can represent highly distinct environments, often harbouring different coral communities. Yet, certain coral species thrive across divergent environments. It is unknown whether the forces of selection are sufficiently strong to overcome the counteracting effects of the typically high gene flow over short distances, and for local adaptation to occur. We screened the coral genome (using restriction site-associated sequencing) and characterized both the dinoflagellate photosymbiont- and tissue-associated prokaryote microbiomes (using metabarcoding) of a reef flat and slope population of the reef-building coral, Pocillopora damicornis, at two locations on Heron Island in the southern Great Barrier Reef. Reef flat and slope populations were separated by <100 m horizontally and ~5 m vertically, and the two study locations were separated by ~1 km. For the coral host, genetic divergence between habitats was much greater than between locations, suggesting limited gene flow between the flat and slope populations. Consistent with environmental selection, outlier loci primarily belonged to the conserved, minimal cellular stress response, likely reflecting adaptation to the different temperature and irradiance regimes on the reef flat and slope. The prokaryote community differed across both habitat and, to a lesser extent, location, whereas the dinoflagellate photosymbionts differed by habitat but not location. The observed intraspecific diversity associated with divergent habitats supports that environmental adaptation involves multiple members of the coral holobiont. Adaptive alleles or microbial associations present in coral populations from the environmentally variable reef flat may provide a source of adaptive variation for assisted evolution approaches, through assisted gene flow, artificial cross-breeding or probiotic inoculations, with the aim to increase climate resilience in the slope populations.
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    Reef invertebrate viromics: diversity, host specificity and functional capacity
    Laffy, PW ; Wood-Charlson, EM ; Turaev, D ; Jutz, S ; Pascelli, C ; Botte, ES ; Bell, SC ; Peirce, TE ; Weynberg, KD ; van Oppen, MJH ; Rattei, T ; Webster, NS (WILEY, 2018-06-01)
    Recent metagenomic analyses have revealed a high diversity of viruses in the pelagic ocean and uncovered clear habitat-specific viral distribution patterns. Conversely, similar insights into the composition, host specificity and function of viruses associated with marine organisms have been limited by challenges associated with sampling and computational analysis. Here, we performed targeted viromic analysis of six coral reef invertebrate species and their surrounding seawater to deliver taxonomic and functional profiles of viruses associated with reef organisms. Sponges and corals' host species-specific viral assemblages with low sequence identity to known viral genomes. While core viral genes involved in capsid formation, tail structure and infection mechanisms were observed across all reef samples, auxiliary genes including those involved in herbicide resistance and viral pathogenesis pathways such as host immune suppression were differentially enriched in reef hosts. Utilising a novel OTU based assessment, we also show a prevalence of dsDNA viruses belonging to the Mimiviridae, Caudovirales and Phycodnaviridae in reef environments and further highlight the abundance of ssDNA viruses belonging to the Circoviridae, Parvoviridae, Bidnaviridae and Microviridae in reef invertebrates. These insights into coral reef viruses provide an important framework for future research into how viruses contribute to the health and evolution of reef organisms.