Reef-building corals provide the foundation for the structural and biological diversity of coral-reef ecosystems. These massive biological structures, which can be seen from space, are the ...culmination of complex interactions between the tiny polyps of the coral animal in concert with its unicellular symbiotic algae and a wide diversity of closely associated microorganisms (bacteria, archaea, fungi, and viruses). While reef-building corals have persisted in various forms for over 200 million years, human-induced conditions threaten their function and persistence. The scope for loss associated with the destruction of coral reef systems is economically, biologically, physically and culturally immense. Here, we provide a micro-to-macro perspective on the biology of scleractinian corals and discuss how cellular processes of the host and symbionts potentially affect the response of these reef builders to the wide variety of both natural and anthropogenic stressors encountered by corals in the Anthropocene. We argue that the internal physicochemical settings matter to both the performance of the host and microbiome, as bio-physical feedbacks may enhance stress tolerance through environmentally mediated host priming and effects on microbiome ecological and evolutionary dynamics.
Putnam et al. review the basic biology of reef-building corals and their symbionts and discuss how our knowledge of these fundamental processes impinges on coral-reef ecology and conservation.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Recent work has shown that hydrophilic and hydrophobic organic matter (OM) from algae disrupts the function of the coral holobiont and promotes the invasion of opportunistic pathogens, leading to ...coral morbidity and mortality. Here we refer to these dynamics as the3 DAM dissolved organic matter (DOM), direct contact, disease, algae and microbes model. There is considerable complexity in coral–algae interactions; turf algae and macroalgae promote heterotrophic microbial overgrowth of coral, macroalgae also directly harm the corals via hydrophobic OM, whereas crustose coralline algae generally encourage benign microbial communities. In addition, complex flow patterns transport OM and pathogens from algae to downstream corals, and direct algal contact enhances their delivery. These invisible players (microbes, viruses, and OM) are important drivers of coral reefs because they have non-linear responses to disturbances and are the first to change in response to perturbations, providing near real-time trajectories for a coral reef, a vital metric for conservation and restoration.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK, ZRSKP
Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize a highly conserved signaling mechanism in which sperm motility is ...stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in early-branching metazoans has remained unexplored. Here, we found that elevating cytoplasmic pH induced a rapid burst of cAMP signaling and triggered the onset of motility in sperm from the reef-building coral
in a sAC-dependent manner. Expression of sAC in the mitochondrial-rich midpiece and flagellum of coral sperm support a dual role for this molecular pH sensor in regulating mitochondrial respiration and flagellar beating and thus motility. In addition, we found that additional members of the homologous signaling pathway described in echinoderms, both upstream and downstream of sAC, are expressed in coral sperm. These include the Na
/H
exchanger SLC9C1, protein kinase A, and the CatSper Ca
channel conserved even in mammalian sperm. Indeed, the onset of motility corresponded with increased protein kinase A activity. Our discovery of this pathway in an early-branching metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize the need to better understand the role of pH-dependent signaling in the reproductive success of marine animals, particularly as climate change stressors continue to alter the physiology of corals and other marine invertebrates.
Symbiotic dinoflagellate algae residing inside coral tissues supply the host with the majority of their energy requirements through the translocation of photosynthetically fixed carbon. The algae, in ...turn, rely on the host for the supply of inorganic carbon. Carbon must be concentrated as CO ₂ in order for photosynthesis to proceed, and here we show that the coral host plays an active role in this process. The host-derived symbiosome membrane surrounding the algae abundantly expresses vacuolar H ⁺-ATPase (VHA), which acidifies the symbiosome space down to pH ∼4. Inhibition of VHA results in a significant decrease in average H ⁺ activity in the symbiosome of up to 75% and a significant reduction in O ₂ production rate, a measure of photosynthetic activity. These results suggest that host VHA is part of a previously unidentified carbon concentrating mechanism for algal photosynthesis and provide mechanistic evidence that coral host cells can actively modulate the physiology of their symbionts.
Significance Coral growth and calcification is supported by sugars acquired from symbiotic algae, allowing corals to thrive in otherwise nutrient-poor environments. This symbiosis depends on the coordinated exchange of compounds between partners, the mechanisms of which are poorly understood. Here we found that coral host cells acidify the microenvironment where the symbiotic algae reside using a proton pump, the V-type H ⁺-ATPase (VHA), which is present in the host membrane surrounding the algae. Acidification of the algal microenvironment by VHA promotes photosynthesis, demonstrating that the coral host can actively regulate symbiont physiology. This work is an important step toward understanding how animal symbioses function and provides mechanistic models that can help understand the capacity of corals to adapt to global climate change.
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Marine heatwaves are occurring more frequently as climate change intensifies, resulting in global mass coral bleaching events several times per decade. Despite the time between marine heatwaves ...decreasing, there is evidence that reef-building corals can develop increased bleaching resistance across repetitive marine heatwaves. This phenomenon of acclimatization via environmental memory may be an important strategy to ensure coral persistence; however, we still understand very little about the apparent acclimatization or, conversely, sensitization (i.e., stress accumulation or weakening) of reef-building corals to consecutive heatwaves and its implications for the trajectory and resilience of coral reefs. Here, we highlight that not only will some corals become stress hardened via marine heatwaves, but many other individuals will suffer sensitization during repeat heatwaves that further exacerbates their stress response during repeat events and depresses fitness. Under current and predicted climate change, it is necessary to gain a better understanding of the acclimatization vs. sensitization trajectories of different species and individuals on the reef, as well as identify whether changes in bleaching susceptibility relates to physiological acclimatization, trade-offs with other biological processes, and ultimately coral persistence in the Anthropocene.
The calcium carbonate skeletons of corals provide the underlying structure of coral reefs; however, the cellular mechanisms responsible for coral calcification remain poorly understood. In ...osteoblasts from vertebrate animals, a Na+/Ca2+ exchanger (NCX) present in the plasma membrane transports Ca2+ to the site of bone formation. The aims of this study were to establish whether NCX exists in corals and its localization within coral cells, which are essential first steps to investigate its potential involvement in calcification. Data mining identified genes encoding for NCX proteins in multiple coral species, a subset of which were more closely related to NCXs from vertebrates (NCXA). We cloned NCXA from Acropora yongei (AyNCXA), which, unexpectedly, contained a peptide signal that targets proteins to vesicles from the secretory pathway. AyNCXA subcellular localization was confirmed by heterologous expression of fluorescently tagged AyNCXA protein in sea urchin embryos, which localized together with known markers of intracellular vesicles. Finally, immunolabeling of coral tissues with specific antibodies revealed AyNCXA was present throughout coral tissue. AyNCXA was especially abundant in calcifying cells, where it exhibited a subcellular localization pattern consistent with intracellular vesicles. Altogether, our results demonstrate AyNCXA is present in vesicles in coral calcifying cells, where potential functions include intracellular Ca2+ homeostasis and Ca2+ transport to the growing skeleton as part of an intracellular calcification mechanism.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. ...Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.
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Increasing ocean temperatures threaten coral reefs globally, but corals residing in habitats that experience high thermal variability are thought to be better adapted to survive climate-induced heat ...stress. Here, we used long-term ecological observations and in situ temperature data from Heron Island, southern Great Barrier Reef to investigate how temperature dynamics within various thermally variable vs. thermally stable reef habitats change during a marine heatwave and the resulting consequences for coral community survival. During the heatwave, thermally variable habitats experienced larger surges in daily mean and maxima temperatures compared to stable sites, including extreme hourly incursions up to 36.5 °C. The disproportionate increase in heat stress in variable habitats corresponded with greater subsequent declines in hard coral cover, including a three-times greater decline within the thermally variable Reef Flat (70%) and Deep Lagoon (83%) than within thermally stable habitats along sheltered and exposed areas of the reef slope (0.3–19%). Interestingly, the thermally variable Reef Crest experienced comparatively small declines (26%), avoiding the most severe tidal ponding and resultant heat stress likely due to proximity to the open ocean equating to lower seawater residence times, greater mixing, and/or increased flow. These results highlight that variable thermal regimes, and any acclimatization or adaptation to elevated temperatures that may lead to, do not necessarily equate to protection against bleaching and mortality during marine heatwaves. Instead, thermally stable habitats that have greater seawater exchange with the open ocean may offer the most protection to corals during the severe marine heatwaves that accompany a changing climate.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Ion transport is fundamental for multiple physiological processes, including but not limited to pH regulation, calcification, and photosynthesis. Here, we investigated ion-transporting processes in ...tissues from the corals Acropora yongei and Stylophora pistillata, representatives of the complex and robust clades that diverged over 250 million years ago. Antibodies against complex IV revealed that mitochondria, an essential source of ATP for energetically costly ion transporters, were abundant throughout the tissues of A. yongei. Additionally, transmission electron microscopy revealed septate junctions in all cell layers of A. yongei, as previously reported for S. pistillata, as well as evidence for transcellular vesicular transport in calicoblastic cells. Antibodies against the alpha subunit of Na(+)/K(+)-ATPase (NKA) and plasma membrane Ca(2+)-ATPase (PMCA) immunolabeled cells in the calicoblastic epithelium of both species, suggesting conserved roles in calcification. However, NKA was abundant in the apical membrane of the oral epithelium in A. yongei but not S. pistillata, while PMCA was abundant in the gastroderm of S. pistillata but not A. yongei. These differences indicate that these two coral species utilize distinct pathways to deliver ions to the sites of calcification and photosynthesis. Finally, antibodies against mammalian sodium bicarbonate cotransporters (NBC; SLC4 family) resulted in strong immunostaining in the apical membrane of oral epithelial cells and in calicoblastic cells in A. yongei, a pattern identical to NKA. Characterization of ion transport mechanisms is an essential step toward understanding the cellular mechanisms of coral physiology and will help predict how different coral species respond to environmental stress.
Identification of a molecular pH sensor in coral Barott, Katie L.; Barron, Megan E.; Tresguerres, Martin
Proceedings of the Royal Society. B, Biological sciences,
11/2017, Volume:
284, Issue:
1866
Journal Article
Peer reviewed
Open access
Maintaining stable intracellular pH (pHi) is essential for homeostasis, and requires the ability to both sense pH changes that may result from internal and external sources, and to regulate ...downstream compensatory pH pathways. Here we identified the cAMP-producing enzyme soluble adenylyl cyclase (sAC) as the first molecular pH sensor in corals. sAC protein was detected throughout coral tissues, including those involved in symbiosis and calcification. Application of a sAC-specific inhibitor caused significant and reversible pHi acidosis in isolated coral cells under both dark and light conditions, indicating sAC is essential for sensing and regulating pHi perturbations caused by respiration and photosynthesis. Furthermore, pHi regulation during external acidification was also dependent on sAC activity. Thus, sAC is a sensor and regulator of pH disturbances from both metabolic and external origin in corals. Since sAC is present in all coral cell types, and the cAMP pathway can regulate virtually every aspect of cell physiology through post-translational modifications of proteins, sAC is likely to trigger multiple homeostatic mechanisms in response to pH disturbances. This is also the first evidence that sAC modulates pHi in any non-mammalian animal. Since corals are basal metazoans, our results indicate this function is evolutionarily conserved across animals.
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