School of BioSciences - Research Publications

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    Microbiome engineering: enhancing climate resilience in corals
    Epstein, HE ; Smith, HA ; Torda, G ; van Oppen, MJH (WILEY, 2019-03)
    The world's coral reefs are under unparalleled pressure due to climate change, stimulating research focused on preventing further damage and loss in these ecosystems. The coral microbiome has been widely acknowledged as crucial to coral health and function, playing multiple roles in key biological processes. Recent empirical studies suggest that microbes may contribute to coral host tolerance of thermal stress, and harnessing these benefits through microbiome engineering (ME) may provide a mechanism for enhancing climate resilience in corals. Although coral ME is in its infancy, similar and successful ME approaches that are already underway in other fields – including agriculture, medicine, and wastewater treatment – may serve to guide and improve ME techniques in corals. We discuss current applications of ME, identify three key research priorities that will help elucidate the viability of ME for corals, and consider the implications of using these approaches for reef restoration.
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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)
    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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    Interspecific gamete compatibility and hybrid larval fitness in reef-building corals: Implications for coral reef restoration
    Chan, WY ; Peplow, LM ; van Oppen, MJH (NATURE PORTFOLIO, 2019-03-18)
    Climate warming is a major cause of the global decline of coral reefs. Active reef restoration, although still in its infancy, is one of several possible ways to help restore coral cover and reef ecosystem function. The deployment of mature coral larvae onto depauperate reef substratum has been shown to significantly increase larval recruitment, providing a novel option for the delivery of ex situ bred coral stock to the reef for restoration purposes. The success of such reef restoration approaches may be improved by the use of coral larval stock augmented for climate resilience. Here we explore whether coral climate resilience can be enhanced via interspecific hybridization through hybrid vigour. Firstly, we assessed cross-fertility of four pairs of Acropora species from the Great Barrier Reef. Temporal isolation in gamete release between the Acropora species was limited, but gametic incompatibility was present with varying strength between species pairs and depending on the direction of the hybrid crosses. We subsequently examined the fitness of hybrid and purebred larvae under heat stress by comparing their survival and settlement success throughout 10 days of exposure to 28 °C, 29.5 °C and 31 °C. Fitness of the majority of Acropora hybrid larvae was similar to that of the purebred larvae of both parental species, and in some instances it was higher than that of the purebred larvae of one of the parental species. Lower hybrid fertilization success did not affect larval fitness. These findings indicate that high hybrid fitness can be achieved after overcoming partial prezygotic barriers, and that interspecific hybridization may be a tool to enhance coral recruitment and climate resilience.
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    Some Rare Indo-Pacific Coral Species Are Probable Hybrids (vol 3, e3240, 2008)
    Richards, ZT ; van Oppen, MJH ; Wallace, CC ; Willis, BL ; Miller, DJ (PUBLIC LIBRARY SCIENCE, 2019-01-25)
    [This corrects the article DOI: 10.1371/journal.pone.0003240.].
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    Temporal Variation in the Microbiome of Acropora Coral Species Does Not Reflect Seasonality
    Epstein, HE ; Smith, HA ; Cantin, NE ; Mocellin, VJL ; Torda, G ; van Oppen, MJH (FRONTIERS MEDIA SA, 2019-08-16)
    The coral microbiome is known to fluctuate in response to environmental variation and has been suggested to vary seasonally. However, most studies to date, particularly studies on bacterial communities, have examined temporal variation over a time frame of less than 1 year, which is insufficient to establish if microbiome variations are indeed seasonal in nature. The present study focused on expanding our understanding of long-term variability in microbial community composition using two common coral species, Acropora hyacinthus, and Acropora spathulata, at two mid-shelf reefs on the Great Barrier Reef. By sampling over a 2-year time period, this study aimed to determine whether temporal variations reflect seasonal cycles. Community composition of both bacteria and Symbiodiniaceae was characterized through 16S rRNA gene and ITS2 rDNA metabarcoding. We observed significant variations in community composition of both bacteria and Symbiodiniaceae among time points for A. hyacinthus and A. spathulata. However, there was no evidence to suggest that temporal variations were cyclical in nature and represented seasonal variation. Clear evidence for differences in the microbial communities found between reefs suggests that reef location and coral species play a larger role than season in driving microbial community composition in corals. In order to identify the basis of temporal patterns in coral microbial community composition, future studies should employ longer time series of sampling at sufficient temporal resolution to identify the environmental correlates of microbiome variation.
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    Scientists' warning to humanity: microorganisms and climate change
    Cavicchioli, R ; Ripple, WJ ; Timmis, KN ; Azam, F ; Bakken, LR ; Baylis, M ; Behrenfeld, MJ ; Boetius, A ; Boyd, PW ; Classen, AT ; Crowther, TW ; Danovaro, R ; Foreman, CM ; Huisman, J ; Hutchins, DA ; Jansson, JK ; Karl, DM ; Koskella, B ; Welch, DBM ; Martiny, JBH ; Moran, MA ; Orphan, VJ ; Reay, DS ; Remais, JV ; Rich, VI ; Singh, BK ; Stein, LY ; Stewart, FJ ; Sullivan, MB ; van Oppen, MJH ; Weaver, SC ; Webb, EA ; Webster, NS (NATURE PORTFOLIO, 2019-09)
    In the Anthropocene, in which we now live, climate change is impacting most life on Earth. Microorganisms support the existence of all higher trophic life forms. To understand how humans and other life forms on Earth (including those we are yet to discover) can withstand anthropogenic climate change, it is vital to incorporate knowledge of the microbial 'unseen majority'. We must learn not just how microorganisms affect climate change (including production and consumption of greenhouse gases) but also how they will be affected by climate change and other human activities. This Consensus Statement documents the central role and global importance of microorganisms in climate change biology. It also puts humanity on notice that the impact of climate change will depend heavily on responses of microorganisms, which are essential for achieving an environmentally sustainable future.
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    The active spread of adaptive variation for reef resilience
    Quigley, KM ; Bay, LK ; van Oppen, MJH (WILEY, 2019-10)
    The speed at which species adapt depends partly on the rates of beneficial adaptation generation and how quickly they spread within and among populations. Natural rates of adaptation of corals may not be able to keep pace with climate warming. Several interventions have been proposed to fast-track thermal adaptation, including the intentional translocation of warm-adapted adults or their offspring (assisted gene flow, AGF) and the ex situ crossing of warm-adapted corals with conspecifics from cooler reefs (hybridization or selective breeding) and field deployment of those offspring. The introgression of temperature tolerance loci into the genomic background of cooler-environment corals aims to facilitate adaptation to warming while maintaining fitness under local conditions. Here we use research on selective sweeps and connectivity to understand the spread of adaptive variants as it applies to AGF on the Great Barrier Reef (GBR), focusing on the genus Acropora. Using larval biophysical dispersal modeling, we estimate levels of natural connectivity in warm-adapted northern corals. We then model the spread of adaptive variants from single and multiple reefs and assess if the natural and assisted spread of adaptive variants will occur fast enough to prepare receiving central and southern populations given current rates of warming. We also estimate fixation rates and spatial extent of fixation under multiple release scenarios to inform intervention design. Our results suggest that thermal tolerance is unlikely to spread beyond northern reefs to the central and southern GBR without intervention, and if it does, 30+ generations are needed for adaptive gene variants to reach fixation even under multiple release scenarios. We argue that if translocation, breeding, and reseeding risks are managed, AGF using multiple release reefs can be beneficial for the restoration of coral populations. These interventions should be considered in addition to conventional management and accompanied by strong mitigation of CO2 emissions.
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    Experimental Inoculation of Coral Recruits With Marine Bacteria Indicates Scope for Microbiome Manipulation in Acropora tenuis and Platygyra daedalea
    Damjanovic, K ; van Oppen, MJH ; Menendez, P ; Blackall, LL (FRONTIERS MEDIA SA, 2019-07-24)
    Coral-associated microorganisms are essential for maintaining the health of the coral holobiont by participating in nutrient cycling and protecting the coral host from pathogens. Under stressful conditions, disruption of the coral prokaryotic microbiome is linked to increased susceptibility to diseases and mortality. Inoculation of corals with beneficial microbes could confer enhanced stress tolerance to the host and may be a powerful tool to help corals thrive under challenging environmental conditions. Here, we explored the feasibility of coral early life stage microbiome manipulation by repeatedly inoculating coral recruits with a bacterial cocktail generated in the laboratory. Co-culturing the two species Acropora tenuis and Platygyra daedalea allowed us to simultaneously investigate the effect of host factors on the coral microbiome. Inoculation cocktails were regularly prepared from freshly grown pure bacterial cultures, which were hence assumed viable, and characterized via the optical density measurement of each individual strain put in suspension. Coral early recruits were inoculated seven times over 3 weeks and sampled once 36 h following the last inoculation event. At this time point, the cumulative inoculations with the bacterial cocktails had a strong effect on the bacterial community composition in recruits of both coral species. While the location of bacterial cells within the coral hosts was not assessed, metabarcoding using the 16S rRNA gene revealed that two and six of the seven bacterial strains administered through the cocktails were significantly enriched in inoculated recruits of A. tenuis and P. daedalea, respectively, compared to control recruits. Despite being reared in the same environment, A. tenuis and P. daedalea established significantly different bacterial communities, both in terms of taxonomic composition and diversity measurements. These findings indicate that coral host factors as well as the environmental bacterial pool play a role in shaping coral-associated bacterial community composition. Host factors may include microbe transmission mode (horizontal versus maternal) and host specificity. While the long-term stability of taxa included in the bacterial inocula as members of the host-associated microbiome remains to be evaluated, our results provide support for the feasibility of coral microbiome manipulation, at least in a laboratory setting.
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    Thermal and Herbicide Tolerances of Chromerid Algae and Their Ability to Form a Symbiosis With Corals
    Chakravarti, LJ ; Negri, AP ; van Oppen, MJH (FRONTIERS MEDIA SA, 2019-02-12)
    Reef-building corals form an obligate symbiosis with photosynthetic microalgae in the family Symbiodiniaceae that meet most of their energy requirements. This symbiosis is under threat from the unprecedented rate of ocean warming as well as the simultaneous pressure of local stressors such as poor water quality. Only 1°C above mean summer sea surface temperatures (SSTs) on the Great Barrier Reef (GBR) can trigger the loss of Symbiodiniaceae from the host, and very low concentrations of the most common herbicide, diuron, can disrupt the photosynthetic activity of microalgae. In an era of rapid environmental change, investigation into the assisted evolution of the coral holobiont is underway in an effort to enhance the resilience of corals. Apicomplexan-like microalgae were discovered in 2008 and the Phylum Chromerida (chromerids) was created. Chromerids have been isolated from corals and contain a functional photosynthetic plastid. Their discovery therefore opens a new avenue of research into the use of alternative/additional photosymbionts of corals. However, only two studies to-date have investigated the symbiotic nature of Chromera velia with corals and thus little is known about the coral-chromerid relationship. Furthermore, the response of chromerids to environmental stressors has not been examined. Here we tested the performance of four chromerid strains and the common dinoflagellate symbiont Cladocopium goreaui (formerly Symbiodinium goreaui, ITS2 type C1) in response to elevated temperature, diuron and their combined exposure. Three of the four chromerid strains exhibited high thermal tolerances and two strains showed exceptional herbicide tolerances, greater than observed for any photosynthetic microalgae, including C. goreaui. We also investigated the onset of symbiosis between the chromerids and larvae of two common GBR coral species under ambient and stress conditions. Levels of colonization of coral larvae with the chromerid strains were low compared to colonization with C. goreaui. We did not observe any overall negative or positive larval fitness effects of the inoculation with chromerid algae vs. C. goreaui. However, we cannot exclude the possibility that chromerid algae may have more important roles in later coral life stages and recommend this be the focus of future studies.
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    The roles of age, parentage and environment on bacterial and algal endosymbiont communities in Acropora corals
    Chan, WY ; Peplow, LM ; Menendez, P ; Hoffmann, AA ; van Oppen, MJH (WILEY, 2019-08)
    The bacterial and microalgal endosymbiont (Symbiodiniaceae spp.) communities associated with corals have important roles in their health and resilience, yet little is known about the factors driving their succession during early coral life stages. Using 16S rRNA gene and ITS2 metabarcoding, we compared these communities in four Acropora coral species and their hybrids obtained from two laboratory crosses (Acropora tenuis × Acropora loripes and Acropora sarmentosa × Acropora florida) across the parental, recruit (7 months old) and juvenile (2 years old) life stages. We tested whether microbiomes differed between (a) life stages, (b) hybrids and purebreds, and (c) treatment conditions (ambient/elevated temperature and pCO2 ). Microbial communities of early life stage corals were highly diverse, lacked host specificity and were primarily determined by treatment conditions. Over time, a winnowing process occurred, and distinct microbial communities developed between the two species pair crosses by 2 years of age, irrespective of hybrid or purebred status. These findings suggest that the microbial communities of corals have a period of flexibility prior to adulthood, which can be valuable to future research aimed at the manipulation of coral microbial communities.