The Precambrian explosion led to the rapid appearance of most major animal phyla alive today. It has been argued that the complexity of life has steadily increased since that event. Here we challenge ...this hypothesis through the characterization of apoptosis in reef-building corals, representatives of some of the earliest animals. Bioinformatic analysis reveals that all of the major components of the death receptor pathway are present in coral with high-predicted structural conservation with Homo sapiens . The TNF receptor-ligand superfamilies (TNFRSF/TNFSF) are central mediators of the death receptor pathway, and the predicted proteome of Acropora digitifera contains more putative coral TNFRSF members than any organism described thus far, including humans. This high abundance of TNFRSF members, as well as the predicted structural conservation of other death receptor signaling proteins, led us to wonder what would happen if corals were exposed to a member of the human TNFSF (HuTNFα). HuTNFα was found to bind directly to coral cells, increase caspase activity, cause apoptotic blebbing and cell death, and finally induce coral bleaching. Next, immortalized human T cells (Jurkats) expressing a functional death receptor pathway (WT) and a corresponding Fas-associated death domain protein (FADD) KO cell line were exposed to a coral TNFSF member (AdTNF1) identified and purified here. AdTNF1 treatment resulted in significantly higher cell death (P < 0.0001) in WT Jurkats compared with the corresponding FADD KO, demonstrating that coral AdTNF1 activates the H. sapiens death receptor pathway. Taken together, these data show remarkable conservation of the TNF-induced apoptotic response representing 550 My of functional conservation.
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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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Variable temperature regimes that expose corals to sublethal heat stress have been recognized as a mechanism to increase coral thermal tolerance and lessen coral bleaching. However, there is a need ...to better understand which thermal regimes maximize coral stress hardening. Here, standardized thermal stress assays were used to determine the relative thermal tolerance of three divergent genera of corals (
Acropora
,
Pocillopora
,
Porites
) originating from six reef sites representing an increasing gradient of annual mean diel temperature fluctuations of 1–3 °C day
−1
. Bleaching severity and dark-acclimated photochemical yield (i.e.,
F
v
/
F
m
) were quantified following exposure to five temperature treatments ranging from 23.0 to 36.3 °C. The greatest thermal tolerance (i.e.,
F
v
/
F
m
effective dose 50) was found at the site with intermediate mean diel temperature variability (2.2 °C day
−1
), suggesting there is an optimal priming exposure that leads to maximal thermal tolerance. Interestingly,
Acropora
and
Pocillopora
originating from the least thermally variable regimes (< 1.3 °C day
−1
) had lower thermal tolerance than corals from the most variable sites (> 2.8 °C day
−1
), whereas the opposite was true for
Porites
, suggesting divergent responses across taxa. Remarkably, comparisons across global studies revealed that the range in coral thermal tolerance uncovered in this study across a single reef (< 5 km) were as large as differences observed across vast latitudinal gradients (300–900 km). This finding indicates that local gene flow could improve thermal tolerance between habitats. However, as climate change continues, exposure to intensifying marine heatwaves is already compromising thermal priming as a mechanism to enhance coral thermal tolerance and bleaching resistance.
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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
Coral and algal holobionts are assemblages of macroorganisms and microorganisms, including viruses, Bacteria, Archaea, protists and fungi. Despite a decade of research, it remains unclear whether ...these associations are spatial-temporally stable or species-specific. We hypothesized that conflicting interpretations of the data arise from high noise associated with sporadic microbial symbionts overwhelming signatures of stable holobiont members. To test this hypothesis, the bacterial communities associated with three coral species (Acropora rosaria, Acropora hyacinthus and Porites lutea) and two algal guilds (crustose coralline algae and turf algae) from 131 samples were analyzed using a novel statistical approach termed the Abundance-Ubiquity (AU) test. The AU test determines whether a given bacterial species would be present given additional sampling effort (that is, stable) versus those species that are sporadically associated with a sample. Using the AU test, we show that coral and algal holobionts have a high-diversity group of stable symbionts. Stable symbionts are not exclusive to one species of coral or algae. No single bacterial species was ubiquitously associated with one host, showing that there is not strict heredity of the microbiome. In addition to the stable symbionts, there was a low-diversity community of sporadic symbionts whose abundance varied widely across individual holobionts of the same species. Identification of these two symbiont communities supports the holobiont model and calls into question the hologenome theory of evolution.
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During the last several decades corals have been in decline and at least one-third of all coral species are now threatened with extinction. Coral disease has been a major contributor to this threat, ...but little is known about the responsible pathogens. To date most research has focused on bacterial and fungal diseases; however, viruses may also be important for coral health. Using a combination of empirical viral metagenomics and real-time PCR, we show that Porites compressa corals contain a suite of eukaryotic viruses, many related to the Herpesviridae. This coral-associated viral consortium was found to shift in response to abiotic stressors. In particular, when exposed to reduced pH, elevated nutrients, and thermal stress, the abundance of herpes-like viral sequences rapidly increased in 2 separate experiments. Herpes-like viral sequences were rarely detected in apparently healthy corals, but were abundant in a majority of stressed samples. In addition, surveys of the Nematostella and Hydra genomic projects demonstrate that even distantly related Cnidarians contain numerous herpes-like viral genes, likely as a result of latent or endogenous viral infection. These data support the hypotheses that corals experience viral infections, which are exacerbated by stress, and that herpes-like viruses are common in Cnidarians.
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Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and ...hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coral
. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures of
sperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.
Significance
Ocean warming has caused catastrophic losses of corals on reefs worldwide and is intensifying faster than the adaptive rate of most coral populations that remain. Human interventions, ...such as propagation of heat-resistant corals, may help maintain reef function and delay further devastation of these valuable ecosystems as society confronts the climate crisis. However, exposing adult corals to a complex suite of new environmental conditions could lead to tradeoffs that alter their heat stress responses, and empirical data are needed to test the utility of this approach. Here, we show that corals transplanted to novel reef conditions did not exhibit changes in their heat stress response or negative fitness tradeoffs, supporting the inclusion of this approach in our management arsenal.
Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change–resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine whether stress resistance is affected by transplantation beyond a coral’s native reef. Here, we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between reefs with distinct pH, salinity, dissolved oxygen, sedimentation, and flow dynamics to determine whether heat stress response is altered following coral exposure to novel physicochemical conditions in situ. Critically, transplantation had no influence on coral heat stress responses, indicating that this trait was relatively fixed. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolic rates and overall fitness were higher at the reef with higher flow, salinity, sedimentation, and diel fluctuations of pH and dissolved oxygen, and did not differ between native and cross-transplanted corals, indicating acclimatization via plasticity within just 3 mo. Conversely, cross-transplants at the second reef had higher fitness than native corals, thus increasing the fitness potential of the recipient population. This experiment was conducted during a nonbleaching year, so the potential benefits to recipient population fitness are likely enhanced during bleaching years. In summary, this study demonstrates that outplanting bleaching-resistant corals is a promising tool for elevating the resistance of coral populations to ocean warming.
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Coral calcification is intricately linked to the chemical composition of the fluid in the extracellular calcifying medium (ECM), which is situated between the calcifying cells and the skeleton. Here ...we demonstrate that the acid-base sensing enzyme soluble adenylyl cyclase (sAC) is expressed in calcifying cells of the coral Stylophora pistillata. Furthermore, pharmacological inhibition of sAC in coral microcolonies resulted in acidification of the ECM as estimated by the pH-sensitive ratiometric indicator SNARF, and decreased calcification rates, as estimated by calcein labeling of crystal growth. These results indicate that sAC activity modulates some of the molecular machinery involved in producing the coral skeleton, which could include ion-transporting proteins and vesicular transport. To our knowledge this is the first study to directly demonstrate biological regulation of the alkaline pH of the coral ECM and its correlation with calcification.
Display omitted
•Soluble adenylyl cyclase (sAC) is an acid-base sensing enzyme.•sAC is present in coral calcifying cells.•sAC activity helps maintain an elevated pH at the site of coral calcification.•sAC activity also influences calcification rate.•Thus, sAC is a molecular mechanism linking coral acid-base sensing to calcification.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Summary
The coral reef benthos is primarily colonized by corals and algae, which are often in direct competition with one another for space. Numerous studies have shown that coral‐associated Bacteria ...are different from the surrounding seawater and are at least partially species specific (i.e. the same bacterial species on the same coral species). Here we extend these microbial studies to four of the major ecological functional groups of algae found on coral reefs: upright and encrusting calcifying algae, fleshy algae, and turf algae, and compare the results to the communities found on the reef‐building coral Montastraea annularis. It was found using 16S rDNA tag pyrosequencing that the different algal genera harbour characteristic bacterial communities, and these communities were generally more diverse than those found on corals. While the majority of coral‐associated Bacteria were related to known heterotrophs, primarily consuming carbon‐rich coral mucus, algal‐associated communities harboured a high percentage of autotrophs. The majority of algal‐associated autotrophic Bacteria were Cyanobacteria and may be important for nitrogen cycling on the algae. There was also a rich diversity of photosynthetic eukaryotes associated with the algae, including protists, diatoms, and other groups of microalgae. Together, these observations support the hypothesis that coral reefs are a vast landscape of distinctive microbial communities and extend the holobiont concept to benthic algae.
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Competition between corals and benthic algae is prevalent on coral reefs worldwide and has the potential to influence the structure of the reef benthos. Human activities may influence the outcome of ...these interactions by favoring algae to become the superior competitor, and this type of change in competitive dynamics is a potential mechanism driving coral–algal phase shifts. Here we surveyed the types and outcomes of coral interactions with benthic algae in the Line Islands of the Central Pacific. Islands ranged from nearly pristine to heavily fished. We observed major differences in the dominant groups of algae interacting with corals between sites, and the outcomes of coral–algal interactions varied across reefs on the different islands. Corals were generally better competitors against crustose coralline algae regardless of location, and were superior competitors against turf algae on reefs surrounding uninhabited islands. On reefs surrounding inhabited islands, however, turf algae were generally the superior competitors. When corals were broken down by size class, we found that the smallest and the largest coral colonies were the best competitors against algae; the former successfully fought off algae while being completely surrounded, and the latter generally avoided algal overgrowth by growing up above the benthos. Our data suggest that human disruption of the reef ecosystem may lead to a building pattern of competitive disadvantage for corals against encroaching algae, particularly turf algae, potentially initiating a transition towards algal dominance.
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