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This study investigates the effects of long-term exposure to OA on skeletal parameters of four tropical zooxanthellate corals naturally living at CO2 seeps and adjacent control sites from two locations (Dobu and Upa Upasina) in the Papua New Guinea underwater volcanic vent system. The seeps are characterized by seawater pH values ranging from 8.0 to about 7.7. The skeletal porosity of Galaxea fascicularis, Acropora millepora, massive Porites, and Pocillopora damicornis was higher (up to ~ 40%, depending on the species) at the seep sites compared to the control sites. Pocillopora damicornis also showed a decrease of micro-density (up to ~ 7%). Thus, further investigations conducted on this species showed an increase of the volume fraction of the larger pores (up to ~ 7%), a decrease of the intraskeletal organic matrix content (up to ~ 15%), and an increase of the intraskeletal water content (up to ~ 59%) at the seep sites. The organic matrix related strain and crystallite size did not vary between seep and control sites. This multi-species study showed a common phenotypic response among different zooxanthellate corals subjected to the same environmental pressures, leading to the development of a more porous skeletal phenotype under OA.

Nitrogen (N) is an essential macronutrient for microalgae, influencing their productivity, composition, and growth dynamics. Despite the dramatic consequences of N starvation, many free-living and endosymbiotic microalgae thrive in N-poor and N-fluctuating environments, giving rise to questions about the existence and nature of their long-term N reserves. Our understanding of these processes requires a unequivocal identification of the N reserves in microalgal cells as well as their turnover kinetics and subcellular localization. Herein, we identified crystalline guanine as the enigmatic large-capacity and rapid-turnover N reserve of microalgae. The identification was unambiguously supported by confocal Raman, fluorescence, and analytical transmission electron microscopies as well as stable isotope labeling. We discovered that the storing capacity for crystalline guanine by the marine dinoflagellate Amphidinium carterae was sufficient to support N requirements for several new generations. We determined that N reserves were rapidly accumulated from guanine available in the environment as well as biosynthesized from various N-containing nutrients. Storage of exogenic N in the form of crystalline guanine was found broadly distributed across taxonomically distant groups of microalgae from diverse habitats, from freshwater and marine free-living forms to endosymbiotic microalgae of reef-building corals (Acropora millepora, Euphyllia paraancora). We propose that crystalline guanine is the elusive N depot that mitigates the negative consequences of episodic N shortage. Guanine (C(5)H(5)N(5)O) may act similarly to cyanophycin (C(10)H(19)N(5)O(5)) granules in cyanobacteria. Considering the phytoplankton nitrogen pool size and dynamics, guanine is proposed to be an important storage form participating in the global N cycle.

Reef-building corals are declining due to environmental changes. Sacsin is a member of the heat shock proteins and has been reported as a candidate protein associated with the stress response inAcroporacorals. Recently, high nucleotide diversity and the persistence of two divergent haplogroups of sacsin-like genes inAcropora milleporahave been reported. While it was not clear when the two haplogroups have split and whether the haplogroups have persisted in onlyA. milleporaor the other lineages in the genusAcropora. In this study, we analyzed a genomic region containing a sacsin-like gene fromAcroporaandMontiporaspecies. Higher nucleotide diversity in the sacsin-like gene compared with that of surrounding regions was also observed inA. digitifera. This nucleotide diversity is derived from two divergent haplogroups of a sacsin-like gene, which are present in at least threeAcroporaspecies. The origin of these two haplogroups can be traced back before the divergence ofAcroporaandMontipora(119 Ma). Although the link between exceptionally high genetic variation in sacsin-like genes and functional differences in sacsin-like proteins is not clear, the divergent haplogroups may respond differently to envionmental stressors and serve in the adaptive phsiological ecology of these keystone species.

Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.

Reef-building corals are cnidarian animals (Anthozoa, Scleractinia) that mostly live in colonies composed of hundreds of thousands of tiny coral polyps. The polyps house dinoflagellate algal photosymbionts of the family Symbiodiniaceae inside their gastrodermal cells (Fig. 1 A ), and this mutualistic association builds the three-dimensional structure of the reefs via deposition of calcium carbonate skeletons. Scleractinian corals thus support a tremendous diversity and biomass of coral reef organisms. However, much of the biology of corals is poorly understood, partly due to a lack of advanced genetic tools for both the corals and the Symbiodiniaceae. In PNAS, Cleves et al. (1) catapult the field forward by describing an efficient protocol for applying the CRISPR technology to the coral Acropora millepora . They show that a CRISPR knockout of the gene encoding Heat Shock Transcription Factor 1 ( HSF1 ) in larvae of this coral reduces their heat shock tolerance, thus confirming a role for HSF1 in protecting corals from heat stress. Fig. 1. The scleractinian coral, Acropora millepora . ( A ) Close-up of individual polyps showing the endosymbiotic Symbiodiniaceae algae as brown pigmentation and as individual cells in the Inset . Symbiodiniaceae cells are ∼5 to 10 µm in diameter. Image credit: Katarina Damjanovic (photographer). ( B ) Bleached and unbleached adult colonies during a natural bleaching event on the Great Barrier Reef. Image credit: Ray Berkelmans (photographer). ( C ) Aposymbiotic larva. Image credit: Kate Quigley (photographer). Gaining a deeper understanding of the coral heat stress response is urgent given that climate warming, and particularly the resulting increased frequency and severity of summer heat waves, are responsible for the alarmingly rapid loss of coral reefs worldwide. Exposure to elevated temperature can result in the loss of the symbiotic algae from the coral … [↵][1]1To whom correspondence may be addressed. Email: madeleine.van{at}unimelb.edu.au. [1]: #xref-corresp-1-1

Rhythms of various periodicities drive cyclical processes in organisms ranging from single cells to the largest mammals on earth, and on scales from cellular physiology to global migrations. The molecular mechanisms that generate circadian behaviours in model organisms have been well studied, but longer phase cycles and interactions between cycles with different periodicities remain poorly understood. Broadcast spawning corals are one of the best examples of an organism integrating inputs from multiple environmental parameters, including seasonal temperature, the lunar phase and hour of the day, to calibrate their annual reproductive event. We present a deep RNA‐sequencing experiment utilizing multiple analyses to differentiate transcriptomic responses modulated by the interactions between the three aforementioned environmental parameters. Acropora millepora was sampled over multiple 24‐hr periods throughout a full lunar month and at two seasonal temperatures. Temperature, lunar and diurnal cycles produce distinct transcriptomic responses, with interactions between all three variables identifying a core set of genes. These core genes include mef2, a developmental master regulator, and two heterogeneous nuclear ribonucleoproteins, one of which is known to post‐transcriptionally interact with mef2 and with biological clock‐regulating mRNAs. Interactions between diurnal and temperature differences impacted a range of core processes ranging from biological clocks to stress responses. Genes involved with developmental processes and transcriptional regulation were impacted by the lunar phase and seasonal temperature differences. Lastly, there was a diurnal and lunar phase interaction in which genes involved with RNA‐processing and translational regulation were differentially regulated. These data illustrate the extraordinary levels of transcriptional variation across time in a simple radial cnidarian in response to the environment under normal conditions.

Neuropeptides play critical roles in cnidarian development. However, although they are known to play key roles in settlement and metamorphosis, their temporal and spatial developmental expression has not previously been characterized in any coral. We here describe Acropora millepora LWamide and RFamide and their developmental expression from the time of their first appearance, using in situ hybridization and FMRFamide immunohistochemistry. AmRFamide transcripts first appear in the ectoderm toward the oral end of the planula larva following blastopore closure. This oral bias becomes less apparent as the planula develops. The cell bodies of AmRFamide-expressing cells are centrally located in the ectoderm, with narrow projections to the mesoglea and to the cell surface. As the planula approaches settlement, AmRFamide expression disappears and is undetectable in the newly settled polyp. Expressing cells then gradually reappear as the polyp develops, becoming particularly abundant on the tentacles. AmLWamide transcripts first appear in ectodermal cells of the developing planula, with minimal expression at its two ends. The cell bodies of expressing cells lie just above the mesoglea, in a position distinct from those of AmRFamide-expressing cells, and have a narrow projection extending across the ectoderm to its surface. AmLWamide-expressing cells persist for most of the planula stage, disappearing shortly before settlement, but later than AmRFamide-expressing cells. As is the case with AmRFamide, expressing cells are absent from the polyp immediately after settlement, reappearing later on its oral side. AmLWamide expression lags that of AmRFamide in both its disappearance and reappearance. Antibodies to FMRFamide stain cells in a pattern similar to that of the transcripts, but also cells in areas where there is no expression revealed by in situ hybridization, most notably at the aboral end of the planula and in the adult polyp. Adult polyps have numerous staining cells on the tentacles and oral discs, as well as an immunoreactive nerve ring around the mouth. There are scattered staining cells in the coenosarc between polyps and staining cells are abundant in the mesenterial filaments. The above results are discussed in the context of our knowledge of the behavior of coral planulae at the time of their settlement and metamorphosis. Corals are facing multiple environmental threats, and these results both highlight the need for, and bring us a step closer to, a mechanistic understanding of a process that is critical to their survival.

Reef-building corals are keystone species that are threatened by anthropogenic stresses including climate change. To investigate corals’ responses to stress and other aspects of their biology, numerous genomic and transcriptomic studies have been performed, generating many hypotheses about the roles of particular genes and molecular pathways. However, it has not generally been possible to test these hypotheses rigorously because of the lack of genetic tools for corals or closely related cnidarians. CRISPR technology seems likely to alleviate this problem. Indeed, we show here that microinjection of single-guide RNA/Cas9 ribonucleoprotein complexes into fertilized eggs of the coral Acropora millepora can produce a sufficiently high frequency of mutations to detect a clear phenotype in the injected generation. Based in part on experiments in a sea-anemone model system, we targeted the gene encoding Heat Shock Transcription Factor 1 (HSF1) and obtained larvae in which >90% of the gene copies were mutant. The mutant larvae survived well at 27 °C but died rapidly at 34 °C, a temperature that did not produce detectable mortality over the duration of the experiment in wild-type (WT) larvae or larvae injected with Cas9 alone. We conclude that HSF1 function (presumably its induction of genes in response to heat stress) plays an important protective role in corals. More broadly, we conclude that CRISPR mutagenesis in corals should allow wide-ranging and rigorous tests of gene function in both larval and adult corals.

A number of tropical reefs have transitioned from coral to macroalgal dominance, but the role of macroalgal competition in coral decline is debated. There is a need to understand the relative roles of direct coral-algal effects versus indirect, microbially mediated effects shaping these interactions, as well as the relevant scales at which interactions operate under natural field, as opposed to laboratory, conditions. We conducted a manipulative field experiment investigating how direct contact versus close proximity (approx. 1.5 cm) with macroalgae ( Galaxaura rugosa , Sargassum polycystum ) impacted the growth, photosynthetic efficiency, and prokaryotic microbiome of the common Indo-Pacific coral Acropora millepora . Both coral growth and photosynthetic efficiency were suppressed when in direct contact with algae or their inert mimics––but not when in close proximity to corals without direct contact. Coral microbiomes were largely unaltered in composition, variability, or diversity regardless of treatment, although a few uncommon taxa differed in abundance among treatments. Negative impacts of macroalgae were contact dependent, accounted for by physical structure alone and had minimal effects on coral microbiomes. The spatial constraints of these interactions have important implications for understanding and predicting benthic community dynamics as reefs degrade.

Elevated suspended sediment concentrations (SSCs) often impact coral fertilisation success, but sediment composition can influence effect thresholds, which is problematic for accurately predicting risk. Here, we derived concentration–response thresholds and cause-effect pathways for SSCs comprising a range of realistic mineral and organic compositions on coral fertilisation success. Effect concentration thresholds (EC10: 10% fertilisation inhibition) varied markedly, with fertilisation highly sensitive to inshore organic-clay rich sediments and bentonite clay at 40 mg L−1). The effect thresholds for relevant sediment types were combined with in situ turbidity data from locations near dredging operations to assess the risks posed by dredging to coral fertilisation at these locations.

The Great Barrier Reef (GBR) is threatened by climate change and local pressures, including contaminants in nearshore habitats. This study investigated the combined effects of a GBR-relevant contaminant, the herbicide diuron, under current and two future climate scenarios on the coral Acropora millepora. All physiological responses tested (effective quantum yield (ΔF/Fm′), photosynthesis, calcification rate) were negatively affected with increasing concentrations of diuron. Interactive effects between diuron and climate were observed for all responses; however, climate had no significant effect on ΔF/Fm′ or calcification rates. Photosynthesis was negatively affected as the climate scenarios were adjusted from ambient (28.1 °C, pCO2 = 397 ppm) to RCP8.5 2050 (29.1 °C, pCO2 = 680 ppm) and 2100 (30.2 °C, pCO2 = 858 ppm) with EC50 values declining from 19.4 to 10.6 and 2.6 μg L−1 diuron in turn. These results highlight the likelihood that water quality guideline values may need to be adjusted as the climate changes.

Successful recruitment in corals is important for the sustenance of coral reefs, and is considered a demographic bottleneck in the recovery of reef populations following disturbance events. Yet several factors influence larval settlement behaviour, and here we quantified thresholds associated with light attenuation and accumulated sediments on settlement substrates. Sediments deposited on calcareous red algae (CRA) directly and indirectly impacted coral settlement patterns. Although not avoiding direct contact, Acropora millepora larvae were very reluctant to settle on surfaces layered with sediments, progressively shifting their settlement preference from upward to downward facing (sediment-free) surfaces under increasing levels of deposited sediment. When only upward-facing surfaces were presented, 10% of settlement was inhibited at thresholds from 0.9 to 16 mg cm− 2 (EC10), regardless of sediment type (carbonate and siliciclastic) or particle size (fine and coarse silt). These levels equate to a very thin (< 150 μm) veneer of sediment that occurs within background levels on reefs. Grooves within settlement surfaces slightly improved options for settlement on sediment-coated surfaces (EC10: 29 mg cm− 2), but were quickly infilled at higher deposited sediment levels. CRA that was temporarily smothered by sediment for 6 d became bleached (53% surface area), and inhibited settlement at ~ 7 mg cm− 2 (EC10). A minor decrease in settlement was observed at high and very low light intensities when using suboptimal concentrations of a settlement inducer (CRA extract); however, no inhibition was observed when natural CRA surfaces along with more realistic diel-light patterns were applied. The low deposited sediment thresholds indicate that even a thin veneer of sediment can have consequences for larval settlement due to a reduction of optimal substrate. And while grooves and overhangs provide more settlement options in high deposition areas, recruits settling at these locations may be subject to ongoing stress from shading, competition, and sediment infilling.

Turbidity associated with elevated suspended sediment concentrations can significantly reduce underwater light availability. Understanding the consequences for sensitive organisms such as corals and crustose coralline algae (CCA), requires an understanding of tolerance levels and the time course of effects. Adult colonies of Acropora millepora and Pocillopora acuta, juvenile P. acuta, and the CCA Porolithon onkodes were exposed to six light treatments of ~0, 0.02, 0.1, 0.4, 1.1 and 4.3 mol photons m−2 d−1, and their physiological responses were monitored over 30 d. Exposure to very low light (-2 d-1) caused tissue discoloration (bleaching) in the corals, and discolouration (and partial mortality) of the CCA, yielding 30 d EI10 thresholds (irradiance which results in a 10% change in colour) of 1.2–1.9 mol photons m−2 d−1. Recent monitoring studies during dredging campaigns on a shallow tropical reef, have shown that underwater light levels very close (~500 m away) from a working dredge routinely fall below this value over 30 d periods, but rarely during the pre-dredging baseline phase. Light reduction alone, therefore, constitutes a clear risk to coral reefs from dredging, although at such close proximity other cause-effect pathways, such as sediment deposition and smothering, are likely to also co-occur.

The interaction between local, anthropogenic stressors, and larger scale regional/global stressors, is often used to explain the current poor condition of many corals reefs. This form of cumulative pressure is clearly manifested by situations where dredging projects happen to coincide with marine heatwaves that have caused coral bleaching. A key pressure associated with dredging is elevated sedimentation. In this study, 3 coral species (Acropora millepora, Porites spp. and Turbinaria reniformis), representing three common morphologies (branching, massive and foliose respectively), were experimentally induced to bleach by exposure to a temperature of 31 °C for 21 d. The corals were then subjected to a range of sedimentation rates (0, 11, 22 and 40 mg cm−2 d−1), and their sediment-rejection ability quantified after 1 and 7 successive sediment deposition events. Bleached corals were less capable of removing sediments from their surfaces, and sediment accumulated 3 to 4-fold more than on normally-pigmented corals. Repeated deposition resulted in a ~3-fold increase in the amount of sediment remaining on the corals, regardless of bleaching status. These results suggest that adaptive management practices need to be developed to reduce the impacts of future dredging projects that follow or coincide with elevated sea surface temperatures and coral bleaching events.

Heat stress is an environmental factor that regularly challenges the well-being of living organisms. This study aims to examine the physiological changes happening in two reef-building coral species exposed to thermal stress under various light conditions. The two ecologically relevant heatwave scenarios were applied under ambient lights (high irradiance) and reduced light conditions (250 and < 10 μmol photons m s). Corals were exposed to elevated temperatures of 32°C (plus 6°) for a period of 1 up to 5 days corresponding to heatwaves reported on the Great Barrier Reef (GBR) that were associated with coral bleaching. We monitored changes in the physiological performance of these two coral species by measuring symbionts and corals’ physiological parameters including symbiont density, levels of multiple algal pigments (chlorophyll a and peridinin), as well as the changes in the host protein concentration. During the short-term heat stress, both species were with stable physiological performance with the only exception of Stylophora pistillata under ambient lights. These results show that S. pistillata was negatively influenced by a synergistic effect of temperature and high irradiance resulting in the first signs of bleaching after only 24h of thermal stress. Exposure to prolonged thermal stress, characterised with a slower rate of temperature increase, affected both coral species investigated and resulted in bleaching mainly by day 5. Interestingly, severe light reduction (

Background Coral reefs can experience salinity fluctuations due to rainfall and runoff; these events can have major impacts on the corals and lead to bleaching and mortality. On the Great Barrier Reef (GBR), low salinity events, which occur during summer seasons and can involve salinity dropping ~ 10 PSU correlate with declines in coral cover, and these events are predicted to increase in frequency and severity under future climate change scenarios. In other marine invertebrates, exposure to low salinity causes increased expression of genes involved in proteolysis, responses to oxidative stress, and membrane transport, but the effects that changes in salinity have on corals have so far received only limited attention. To better understand the coral response to hypo-osmotic stress, here we investigated the transcriptomic response of the coral Acropora millepora in both adult and juvenile life stages to acute (1 h) and more prolonged (24 h) exposure to low salinity. Results Differential gene expression analysis revealed the involvement of both common and specific response mechanisms in Acropora. The general response to environmental stressors included up-regulation of genes involved in the mitigation of macromolecular and oxidative damage, while up-regulation of genes involved in amino acid metabolism and transport represent specific responses to salinity stress. Conclusions This study is the first comprehensive transcriptomic analysis of the coral response to low salinity stress and provides important insights into the likely consequences of heavy rainfall and runoff events on coral reefs. Electronic supplementary material The online version of this article (10.1186/s12864-019-5527-2) contains supplementary material, which is available to authorized users.

Reef restoration efforts, utilising sexual coral propagation need up-scaling to have ecologically meaningful impact. Post-settlement survival bottlenecks, in part due to competitive benthic algae interactions should be addressed, to improve productivity for these initiatives. Sea urchins are keystone grazers in reef ecosystems, yet feeding behaviour of adults causes physical damage and mortality to developing coral spat. To investigate if microherbivory can be utilised for co-culture, we quantitatively assessed how varying densities of juvenile sea urchins Mespilia globulus (Linnaeus, 1758), reared alongside the coral Acropora millepora (Ehrenberg, 1834) effected survival and growth of coral recruits. Spawning of both species were induced ex situ. A comparison of A. millepora spat reared in three M. globulus densities (low 16.67 m−2, medium 37.50 m−2, high 75.00 m−2) and a non-grazed control indicated coral survival is significantly influenced by grazing activity (p p

[Excerpt] Reef-building corals are iconic animals that are in global decline as a consequence of increasing anthropogenic pressure, but the development of strategies to ensure their conservation is constrained by our limited understanding of the molecular bases of many aspects of coral biology. Some coral genera are particularly sensitive to stress and, among these, Acropora is of particular significance because this is the dominant genus of reef-building corals in the Indo-Pacific. These factors have led to members of this genus often being the subjects of investigation into coral responses to various physical and biological stressors. Fittingly, the first coral genome to be sequenced was Acropora digitifera; the availability of this whole-genome sequence (Shinzato et al. 2011) allowed substantial progress in several areas of coral biology, including the molecular underpinnings of symbiosis and calcification (Hamada et al. 2013; Ramos-Silva et al. 2013). Here we report the whole-genome sequence of a second Acropora species, A. millepora, which has been the most extensively studied Acropora species at the molecular level (reviewed in Miller et al. 2011) by virtue of its wide distribution (Carpenter et al. 2008; Madin et al. 2016) and the ease with which it can be identified in what is a highly speciose genus.

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness-related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef-building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade-offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals' adaptive capacity when predicting the future of coral reefs.

Coral reef replenishment is threatened by global climate change and local water-quality degradation, including smothering of coral recruits by sediments generated by anthropogenic activities. Here we show that the ability of Acropora millepora recruits to remove sediments diminishes under future climate conditions, leading to increased mortality. Recruits raised under future climate scenarios for fourteen weeks (highest treatment: +1.2 °C, pCO2: 950 ppm) showed twofold higher mortality following repeated sediment deposition (50% lethal sediment concentration LC50: 14–24 mg cm−2) compared to recruits raised under current climate conditions (LC50: 37–51 mg cm−2), depending on recruit age at the time of sedimentation. Older and larger recruits were more resistant to sedimentation and only ten-week-old recruits grown under current climate conditions survived sediment loads possible during dredging operations. This demonstrates that water-quality guidelines for managing sediment concentrations will need to be climate-adjusted to protect future coral recruitment.

Gene expression biomarkers (GEBs) are emerging as powerful diagnostic tools for identifying and characterizing coral stress. Their capacity to detect sublethal stress prior to the onset of signs at the organismal level that might already indicate significant damage makes them more precise and proactive compared to traditional monitoring techniques. A high number of candidate GEBs, including certain heat shock protein genes, metabolic genes, oxidative stress genes, immune response genes, ion transport genes, and structural genes have been investigated, and some genes, including hsp16, Cacna1, MnSOD, SLC26, and Nf-kB, are already showing excellent potential as reliable indicators of thermal stress in corals. In this mini-review, we synthesize the current state of knowledge of scleractinian coral GEBs and highlight gaps in our understanding that identify directions for future work. We also address the underlying sources of variation that have sometimes led to contrasting results between studies, such as differences in experimental set-up and approach, intrinsic variation in the expression profiles of different experimental organisms (such as between different colonies or their algal symbionts), diel cycles, varying thermal history, and different expression thresholds. Despite advances in our understanding there is still no universally accepted biomarker of thermal stress, the molecular response of corals to heat stress is still unclear, and biomarker research in Symbiodinium still lags behind that of the host. These gaps should be addressed in future work.

Corals are fundamental ecosystem engineers, creating large, intricate reefs that support diverse and abundant marine life. At the core of a healthy coral animal is a dynamic relationship with microorganisms, including a mutually beneficial symbiosis with photosynthetic dinoflagellates (Symbiodinium spp.) and enduring partnerships with an array of bacterial, archaeal, fungal, protistan, and viral associates, collectively termed the coral holobiont. The combined genomes of this coral holobiont form a coral hologenome, and genomic interactions within the hologenome ultimately define the coral phenotype. Here we integrate contemporary scientific knowledge regarding the ecological, host-specific, and environmental forces shaping the diversity, specificity, and distribution of microbial symbionts within the coral holobiont, explore physiological pathways that contribute to holobiont fitness, and describe potential mechanisms for holobiont homeostasis. Understanding the role of the microbiome in coral resilience, acclimation, and environmental adaptation is a new frontier in reef science that will require large-scale collaborative research efforts.

A candidate antimicrobial peptide (AmAMP1) was identified by searching the whole genome sequence of Acropora millepora for short (

Coral reefs of the North Indo-West Pacific provide important ecosystem services to the region but are subjected to multiple local and global threats. Strengthening management measures necessitate understanding the variability of larval connectivity and bridging global connectivity models to local scales. An individual-based Lagrangian biophysical model was used to simulate connectivity between coral reefs for three organisms with different early life history characteristics: a coral (Acropora millepora), a sea urchin (Tripneustes gratilla), and a reef fish (Epinephelus sp). Connectivity metrics and reef clusters were computed from the settlement probability matrices. Fitted power law functions derived from the dispersal kernels provided relative probabilities of connection given only the distance between reefs, and demonstrated that 95% of the larvae across organisms settled within a third of their maximum settlement distances. The magnitude of the connectivity metric values of reef cells were sensitive to differences both in the type of organism and temporal variability. Seasonal variability of connections was more dominant than interannual variability. However, despite these differences, the moderate to high correlation of metrics between organisms and seasonal matrices suggest that the spatial patterns are relatively similar between reefs. A cluster analysis based on the Bray-Curtis Dissimilarity of sink and source connections synthesized the inherent variability of these multiple large connectivity matrices. Through this, similarities in regional connectivity patterns were determined at various cluster sizes depending on the scale of interest. The validity of the model is supported by 1) the simulated dispersal kernels being within the range of reported parentage analysis estimates; and, 2) the clusters that emerged reflect the dispersal barriers implied by previously published population genetics studies. The tools presented here (dispersal kernels, temporal variability maps and reef clustering) can be used to include regional patterns of connectivity into the spatial management of coral reefs.

Phototrophic sessile organisms, such as reef corals, adjust their photosynthetic apparatus to optimize the balance of light capture versus protection in response to variable light availability (photoacclimation). In shallow marine environments, daily light integrals (DLI) can vary several-fold in response to water clarity and clouds. This laboratory study investigated the responses of two coral species to fluctuations in DLI. Corals were exposed to four contrasting DLI treatments: 'high-light' (potentially photoinhibiting conditions, 32 mol photons m-2 d-1), 'low-light' (potentially light-limiting conditions, 6 mol photons m-2 d-1), and two 'variable light' treatments that alternated between high and low conditions every 5 days. In the variable treatments, the shade-tolerant coral Pachyseris speciosa displayed cycles of rapid declines in maximum quantum yield during high-light and subsequent recoveries during low-light, showing photoacclimation at a time scale of 3-5 days. In contrast, the shallow-water coral Acropora millepora showed slow (>20 days) photoacclimation, and minimal changes in photosynthetic yields despite contrasting light exposure. However, growth (change in buoyant weight) in A. millepora was significantly slower under variable light, and even more so under low-light conditions, compared with high-light conditions. The responses of yields in P. speciosa match their preference for low-light environments, but suggest a vulnerability to even short periods of high-light exposure. In contrast, A. millepora had better tolerance of high-light conditions, however its slow photoacclimatory responses limit its growth under low and variable conditions. The study shows contrasting photoacclimatory responses in variable light environments, which is important to identify and understand as many coastal and midshelf reefs are becoming increasingly more turbid, and may experience higher variability in light availability.

Coral reefs are declining dramatically and losing species richness, but the impact of declining biodiversity on coral well-being remains inadequately understood. Here, we demonstrate that lower coral species richness alone can suppress the growth and survivorship of multiple species of corals (Porites cylindrica, Pocillopora damicornis and Acropora millepora) under field conditions on a degraded, macroalgae-dominated reef. Our findings highlight the positive role of biodiversity in the function of coral reefs, and suggest that the loss of coral species richness may trigger negative feedback that causes further ecosystem decline. Sixteen-month manipulation experiments in a degraded macroalgae-dominated tropical reef setting show that lower coral species richness suppresses growth and survivorship of multiple species.

Oil spill responders require information on the absolute and relative toxicities of chemical dispersants to relevant receptor species to assess their use in spill response. However, little toxicity data are available for tropical marine species including reef-building corals. In this study, we experimentally assessed the sub-lethal toxicity of five dispersants to larvae of the coral Acropora millepora over three short exposure periods (2, 6 and 24 h) reflecting real-world spill response scenario durations. Inhibition of larval settlement increased rapidly between 2 and 6 h, and was highest at 24 h: EC50 Corexit EC9500A = 4.0 mg l−1; Ardrox 6120 = 4.0 mg l−1; Slickgone LTSW = 2.6 mg L−1; Slickgone NS = 11.1 mg L−1 and Finasol OSR52 = 3.4 mg L−1. Coral larvae were more sensitive to dispersants than most other coral life stages and marine taxa, but the toxic thresholds (EC10s) exceeded most realistic environmental dispersant concentrations. Estimating toxic threshold values for effects of dispersants on coral should benefit the decision-making of oil spill responders by contributing to the development of species sensitivity distributions (SSDs) for dispersant toxicity, and by informing net environmental benefit assessment (NEBA) for dispersant use.

Diazotrophic bacteria are instrumental in generating biologically usable forms of nitrogen by converting abundant dinitrogen gas (N-2) into available forms, such as ammonium. Although nitrogen is crucial for coral growth, direct observation of associations between diazotrophs and corals has previously been elusive. We applied fluorescence in situ hybridization (FISH) and nanoscale secondary ion mass spectrometry to observe the uptake of N-15-enriched diazotrophic Vibrio sp. isolated from Acropora millepora into conspecific coral larvae. Incorporation of Vibrio sp. cells was observed in coral larvae after 4-h incubation with enriched bacteria. Uptake was restricted to the aboral epidermis of larvae, where Vibrio cells clustered in elongated aggregations. Other bacterial associates were also observed in epidermal areas in FISH analyses. Although the fate and role of these bacteria requires additional investigation, this study describes a powerful approach to further explore cell associations and nutritional pathways in the early life stages of the coral holobiont.

Around volcanic carbon dioxide (CO2) seeps in Papua New Guinea, partial pressures of CO2 (pCO2) approximate those as predicted for the end of this century, and coral communities have low diversity and low structural complexity. To assess the mechanisms for such community shifts in response to ocean acidification, we examined the physiological performance of two hard corals that occur with increased or unaltered abundance at a seep site (mean pHTotal=7.8, pCO2=862 μatm) compared to a control site (mean pHTotal=8.1, pCO2=323 μatm), namely massive Porites spp. and Pocillopora damicornis, and two species with reduced abundance, Acropora millepora and Seriatopora hystrix. Oxygen fluxes, calcification, and skeletal densities were analyzed in corals originating from the seep and control site. Net photosynthesis rates increased considerably in Porites spp. and A. millepora and slightly in P. damicornis at increased pCO2, but remained unaltered in S. hystrix. Dark respiration rates remained constant in all corals investigated from both sites. Rates of light calcification declined in S. hystrix at high pCO2, but were unaffected by pCO2 in the other three coral taxa. Dark and net calcification rates remained unchanged in massive Porites and P. damicornis, but were drastically reduced at high pCO2 in A. millepora and S. hystrix. However, skeletal densities were similar at both seep and control sites in all coral taxa investigated. Our data suggest that the pCO2-tolerant corals were characterized by an increased ability to acclimatize to ocean acidification, e.g. by maintaining net calcification. Thus, robust corals, such as Porites spp. and P. damicornis, are more likely to persist for longer in a future high pCO2 world than those unable to acclimatize.

Background Molecular mechanisms underlying coral larval competence, the ability of larvae to respond to settlement cues, determine their dispersal potential and are potential targets of natural selection. Here, we profiled competence, fluorescence and genome-wide gene expression in embryos and larvae of the reef-building coral Acropora millepora daily throughout 12 days post-fertilization. Results Gene expression associated with competence was positively correlated with transcriptomic response to the natural settlement cue, confirming that mature coral larvae are “primed” for settlement. Rise of competence through development was accompanied by up-regulation of sensory and signal transduction genes such as ion channels, genes involved in neuropeptide signaling, and G-protein coupled receptor (GPCRs). A drug screen targeting components of GPCR signaling pathways confirmed a role in larval settlement behavior and metamorphosis. Conclusions These results gives insight into the molecular complexity underlying these transitions and reveals receptors and pathways that, if altered by changing environments, could affect dispersal capabilities of reef-building corals. In addition, this dataset provides a toolkit for asking broad questions about sensory capacity in multicellular animals and the evolution of development. Electronic supplementary material The online version of this article (10.1186/s12864-017-4392-0) contains supplementary material, which is available to authorized users.

Developing an optimal heterotrophic feeding regime has the potential to improve captive coral growth and health. This study evaluated the efficacy of three exogenous diets: Artemia nauplii (ART), a commercially available coral diet (Reef Roids) (RR), and a novel, micro-bound diet (ATF), against a comparatively natural, unfiltered seawater treatment (RAW), and an unfed, ultra-filtered seawater treatment (CTL), in adult Acropora millepora and Pocillopora acuta nubbins. After 90 days, both species showed significantly positive weight gain in response to one treatment (A. millepora–RAW, P. acuta–ART), and comparatively low growth in response to another (A. millepora–ATF, P. acuta–RR). The results highlighted substantial differences in the nutritional requirements between species. The nutritional composition of A. millepora in the best performing treatment was dominated by high-energy materials such as storage lipids and saturated and monounsaturated fatty acids. In contrast, the P. acuta nutritional profile in the superior treatment showed a predominance of structural materials, including protein, phospholipids, and polyunsaturated fatty acids. This study demonstrates that Artemia nauplii can successfully replace a natural feeding regime for captive P. acuta, yet highlights the considerable work still required to optimise supplementary feeding regimes for A. millepora.

International audience; The grazing activity by specific marine organisms represents a growing threat to the survival of many scleractinian species. For example, the recent proliferation of the corallivorous gastropod Drupella now constitutes a critical case in all South-East Asian waters. If the damaging effects caused by this marine snail on coral polyps are relatively well known, the indirect incidence of predation on coral microbial associates is still obscure and might also potentially impair coral health. In this study, we compared the main ecological traits of coral-associated bacterial and viral communities living in the mucus layer of Acropora formosa and Acropora millepora, of healthy and predated individuals (i.e., colonized by Drupella rugosa), in the Bay of Van Phong (Vietnam). Our results show a substantial impact of the gastropod on a variety of microbiological markers. Colonized corals harbored much more abundant and active epibiotic bacteria whose community composition shifted toward more pathogenic taxa (belonging to the Vibrionales, Clostridiales, Campylobacterales, and Alteromonadales orders), together with their specific phages. Viral epibionts were also greatly influenced by Drupella corallivory with spectacular modifications in their concentrations, life strategies, genotype richness, and diversity. Novel and abundant circular Rep-encoding ssDNA viruses (CRESS-DNA viruses) were detected and characterized in grazed corals and we propose that their occurrence may serve as indicator of the coral health status. Finally, our results reveal that corallivory can cause severe dysbiosis by altering virus-bacteria interactions in the mucus layer, and ultimately favoring the development of local opportunistic infections.

Reef-building corals can increase their resistance to heat-induced bleaching through adaptation and acclimatization and/or by associating with a more thermo-tolerant strain of algal symbiont (Symbiodinium sp.). Here, we show that these two adaptive pathways interact. We collected Acropora millepora corals from two contrasting thermal environments on the Great Barrier Reef: cooler, mid-latitude Orpheus Island, where all corals hosted a heat-sensitive clade C Symbiodinium, and warmer, low-latitude Wilkie Island, where corals hosted either a clade C or a more thermo-tolerant clade D. Corals were kept in a benign common garden to reveal differences in baseline gene expression, reflecting prior adaptation/long-term acclimatization. Model-based analysis identified gene expression differences between Wilkie and Orpheus corals that were negatively correlated with previously described transcriptome-wide signatures of heat stress, signifying generally elevated thermotolerance of Wilkie corals. Yet, model-free analyses of gene expression revealed that Wilkie corals hosting clade C were distinct from Wilkie corals hosting clade D, whereas Orpheus corals were more variable. Wilkie corals hosting clade C symbionts exhibited unique functional signatures, including downregulation of histone proteins and ion channels and upregulation of chaperones and RNA processing genes, putatively representing constitutive "frontloading" of stress response genes. Furthermore, clade C Symbiodinium exhibited constitutive expression differences between Wilkie and Orpheus, indicative of contrasting life history strategies. Our results demonstrate that hosting alternative Symbiodinium types is associated with different pathways of local adaptation for the coral host. These interactions could play a significant role in setting the direction of genetic adaptation to global warming in the two symbiotic partners.

Background Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching. Results Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata. Conclusions We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral’s antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress. Electronic supplementary material The online version of this article (doi:10.1186/s12915-017-0459-2) contains supplementary material, which is available to authorized users.

Disease causes significant coral mortality worldwide; however, factors responsible for intraspecific variation in disease resistance remain unclear. We exposed fragments of eight Acropora millepora colonies (genotypes) to putatively pathogenic bacteria (Vibrio spp.). Genotypes varied from zero to >90% mortality, with bacterial challenge increasing average mortality rates 4–6 fold and shifting the microbiome in favor of stress-associated taxa. Constitutive immunity and subsequent immune and transcriptomic responses to the challenge were more prominent in high-mortality individuals, whereas low-mortality corals remained largely unaffected and maintained expression signatures of a healthier condition (i.e., did not launch a large stress response). Our results suggest that lesions appeared due to changes in the coral pathobiome (multiple bacterial species associated with disease) and general health deterioration after the biotic disturbance, rather than the direct activity of any specific pathogen. If diseases in nature arise because of weaknesses in holobiont physiology, instead of the virulence of any single etiological agent, environmental stressors compromising coral condition might play a larger role in disease outbreaks than is currently thought. To facilitate the diagnosis of compromised individuals, we developed and independently cross-validated a biomarker assay to predict mortality based on genes whose expression in asymptomatic individuals coincides with mortality rates.

The highly conserved ADAR enzymes, found in all multicellular metazoans, catalyze the editing of mRNA transcripts by the deamination of adenosines to inosines. This type of editing has two general outcomes: site specific editing, which frequently leads to recoding, and clustered editing, which is usually found in transcribed genomic repeats. Here, for the first time, we looked for both editing of isolated sites and clustered, non-specific sites in a basal metazoan, the coral Acropora millepora during spawning event, in order to reveal its editing pattern. We found that the coral editome resembles the mammalian one: it contains more than 500,000 sites, virtually all of which are clustered in non-coding regions that are enriched for predicted dsRNA structures. RNA editing levels were increased during spawning and increased further still in newly released gametes. This may suggest that editing plays a role in introducing variability in coral gametes.

Background Dimethylsulfoniopropionate (DMSP) is a small sulphur compound which is produced in prodigious amounts in the oceans and plays a pivotal role in the marine sulfur cycle. Until recently, DMSP was believed to be synthesized exclusively by photosynthetic organisms; however we now know that corals and specific bacteria can also produce this compound. Corals are major sources of DMSP, but the molecular basis for its biosynthesis is unknown in these organisms. Results Here we used salinity stress, which is known to trigger DMSP production in other organisms, in conjunction with transcriptomics to identify coral genes likely to be involved in DMSP biosynthesis. We focused specifically on both adults and juveniles of the coral Acropora millepora: after 24 h of exposure to hyposaline conditions, DMSP concentrations increased significantly by 2.6 fold in adult corals and 1.2 fold in juveniles. Concomitantly, candidate genes enabling each of the necessary steps leading to DMSP production were up-regulated. Conclusions The data presented strongly suggest that corals use an algal-like pathway to generate DMSP from methionine, and are able to rapidly change expression of the corresponding genes in response to environmental stress. However, our data also indicate that DMSP is unlikely to function primarily as an osmolyte in corals, instead potentially serving as a scavenger of ROS and as a molecular sink for excess methionine produced as a consequence of proteolysis and osmolyte catabolism in corals under hypo-osmotic conditions. Electronic supplementary material The online version of this article (doi:10.1186/s12864-017-3959-0) contains supplementary material, which is available to authorized users.

Atmospheric carbon dioxide (CO2) levels are rapidly rising causing an increase in the partial pressure of CO2 (pCO2) in the ocean and a reduction in pH known as ocean acidification (OA). Natural volcanic seeps in Papua New Guinea expel 99% pure CO2 and thereby offer a unique opportunity to explore the effects of OA in situ. The corals Acropora millepora and Porites cylindrica were less abundant and hosted significantly different microbial communities at the CO2 seep than at nearby control sites

Early establishment of coral-microbial symbioses is fundamental to the fitness of corals, but comparatively little is known about the onset and succession of bacterial communities in their early life history stages. In this study, bacterial associates of the coral Acropora millepora were characterized throughout the first year of life, from larvae and 1-week-old juveniles reared in laboratory conditions in the absence of the dinoflagellate endosymbiont Symbiodinium to field-outplanted juveniles with established Symbiodinium symbioses, and sampled at 2 weeks and at 3, 6 and 12 months. Using an amplicon pyrosequencing approach, the diversity of both nitrogen-fixing bacteria and of bacterial communities overall was assessed through analysis of nifH and 16S rRNA genes, respectively. The consistent presence of sequences affiliated with diazotrophs of the order Rhizobiales (23-58% of retrieved nifH sequences; 2-12% of 16S rRNA sequences), across all samples from larvae to 12-month-old coral juveniles, highlights the likely functional importance of this nitrogen-fixing order to the coral holobiont. Dominance of Roseobacter-affiliated sequences (55% of retrieved 16S rRNA sequences) in larvae and 1-week-old juveniles, and the consistent presence of sequences related to Oceanospirillales and Altermonadales throughout all early life history stages, signifies their potential importance as coral associates. Increased diversity of bacterial communities once juveniles were transferred to the field, particularly of Cyanobacteria and Deltaproteobacteria, demonstrates horizontal (environmental) uptake of coral-associated bacterial communities. Although overall bacterial communities were dynamic, bacteria with likely important functional roles remain stable throughout early life stages of Acropora millepora.