Calcium homeostasis disruption initiates rapid growth after micro-fragmentation in the scleractinian coral Porites lobata.

Coral reefs are ecosystems under increasing threat from global climate change. Coral restoration is a tool for preserving the biological and ecological function of coral reefs by mitigating coral loss and maintaining the structural integrity and complexity of reefs. To generate the necessary stock for coral restoration, larger coral colonies are usually fragmented to generate smaller specimens for outplanting, taking advantage of the high regenerative ability of corals. In this study, we utilized RNA-seq technology to understand the physiological responses of Porites lobata colonies to physical fragmentation and outplanting, which have thus far not been characterized. Our results demonstrate that P. lobata fragments undergoing physical injury recover through two distinct phases: rapid wound regeneration of the cut margins, followed by a slower growth phase that cements the colony to the substrate. Our study found rapid physiological responses to acute physical injury and outplanting in the coral host that involved significantly increased energy production, calcium homeostasis disruption, and endoplasmic reticulum (ER) stress leading to increased antioxidant expression and rates of protein turnover. Our results suggest that phosphoinositide-mediated acute calcium homeostasis disruption stimulates wound recovery processes in response to physical injury. Symbiont gene expression revealed extremely low gene differences in response to fragmentation, growth, and outplanting. These results provide insight into the physiological mechanisms that allow for rapid wound healing and stabilization in response to physical injury in corals.

Going with the flow: How corals in high-flow environments can beat the heat.

Coral reefs are experiencing unprecedented declines in health on a global scale leading to severe reductions in coral cover. One major cause of this decline is increasing sea surface temperature. However, conspecific colonies separated by even small spatial distances appear to show varying responses to this global stressor. One factor contributing to differential responses to heat stress is variability in the coral's micro-environment, such as the amount of water flow a coral experiences. High flow provides corals with a variety of health benefits, including heat stress mitigation. Here, we investigate how water flow affects coral gene expression and provides resilience to increasing temperatures. We examined host and photosymbiont gene expression of Acropora cf. pulchra colonies in discrete in situ flow environments during a natural bleaching event. In addition, we conducted controlled ex situ tank experiments where we exposed A. cf. pulchra to different flow regimes and acute heat stress. Notably, we observed distinct flow-driven transcriptomic signatures related to energy expenditure, growth, heterotrophy and a healthy coral host-photosymbiont relationship. We also observed disparate transcriptomic responses during bleaching recovery between the high- and low-flow sites. Additionally, corals exposed to high flow showed "frontloading" of specific heat-stress-related genes such as heat shock proteins, antioxidant enzymes, genes involved in apoptosis regulation, innate immunity and cell adhesion. We posit that frontloading is a result of increased oxidative metabolism generated by the increased water movement. Gene frontloading may at least partially explain the observation that colonies in high-flow environments show higher survival and/or faster recovery in response to bleaching events.

Chemical and Metagenomic Studies of the Lethal Black Band Disease of Corals Reveal Two Broadly Distributed, Redox-Sensitive Mixed Polyketide/Peptide Macrocycles.

Black band disease (BBD), a lethal, polymicrobial disease consortium dominated by the cyanobacterium Roseofilum reptotaenium, kills many species of corals worldwide. To uncover chemical signals or cytotoxins that could be important in proliferation of Roseofilum and the BBD layer, we examined the secondary metabolites present in geographically diverse collections of BBD from Caribbean and Pacific coral reefs. Looekeyolide A (1), a 20-membered macrocyclic compound formed by a 16-carbon polyketide chain, 2-deamino-2-hydroxymethionine, and d-leucine, and its autoxidation product looekeyolide B (2) were extracted as major compounds (∼1 mg g-1 dry wt) from more than a dozen field-collected BBD samples. Looekeyolides A and B were also produced by a nonaxenic R. reptotaenium culture under laboratory conditions at similar concentrations. R. reptotaenium genomes that were constructed from four different metagenomic data sets contained a unique nonribosomal peptide/polyketide biosynthetic cluster that is likely responsible for the biosynthesis of the looekeyolides. Looekeyolide A, which readily oxidizes to looekeyolide B, may play a biological role in reducing H2O2 and other reactive oxygen species that could occur in the BBD layer as it overgrows and destroys coral tissue.

Whale Shark Tourism: Impacts on Coral Reefs in the Philippines.

Reef-based tourism has been developing rapidly in recent decades yet its impacts on reef ecosystems are often overlooked. In Tan-awan, Oslob, Philippines, whale sharks are attracted to the shallow reefs where they are provisioned up to 50 tons y-1 of feed and this phenomenon in turn attracts >300,000 y-1 visitors. Given the intensive provisioning and concentrating tourism activities, we hypothesized that the whale shark tourism-impacted site (IS) will have greater impacts on reef degradation and higher anthropogenic nitrogen pollution level compared to its reference site (RS). Ecological surveys revealed that relative to the RS, the IS had 36% higher relative abundance of Pocillopora and Porites coral over other genera, >2.5-fold lower coral density, and 20% higher macroalgal cover, which we concluded are signs of reef degradation. Also, we conducted stable nitrogen isotope analysis on gorgonian skeletons to trace nitrogen sources at both sites through time. Although an average 1‰ isotope enrichment found in the IS relative to the RS could indicate anthropogenic nitrogen inputs in the IS, this enrichment was consistent over time and existed before the tourism developed. Despite that, we cautioned against the imminent threat of local eutrophication caused by the continued inputs of nitrogen derived from provisioning and tourism activities. In summary, this study provided the first documentation of the impacts of provisioned whale shark tourism on the local reefs in Tan-awan and established an ecological baseline for future comparisons. Such assessments can offer important information on reef health, coastal development, and tourism management.

Life and death of a sewage treatment plant recorded in a coral skeleton δ15N record.

We investigated the potential of coral skeleton δ15N (CS-δ15N) records for tracking anthropogenic-N sources in coral reef ecosystems. We produced a 56yr-long CS-δ15N record (1958-2014) from a reef flat in Guam that has been exposed to varying 1) levels of sewage treatment 2) population density, and 3) land use. Increasing population density (from <30 to 300ind·km-2) and land use changes in the watershed resulted in a ~1‰ enrichment of the CS-δ15N record until a sewage treatment plant (STP) started operation in 1975. Then, CS-δ15N stabilized, despite continued population density and land use changes. Based on population and other considerations, a continued increase in the sewage footprint might have been expected over this time. The stability of CS-δ15N, either contradicts this expectation, or indicates that the impacts on the outer reef at the coring site were buffered by the mixing of reef water with the open ocean.

Comparative Metagenomics of the Polymicrobial Black Band Disease of Corals.

Black Band Disease (BBD), the destructive microbial consortium dominated by the cyanobacterium Roseofilum reptotaenium, affects corals worldwide. While the taxonomic composition of BBD consortia has been well-characterized, substantially less is known about its functional repertoire. We sequenced the metagenomes of Caribbean and Pacific black band mats and cultured Roseofilum and obtained five metagenome-assembled genomes (MAGs) of Roseofilum, nine of Proteobacteria, and 12 of Bacteroidetes. Genomic content analysis suggests that Roseofilum is a source of organic carbon and nitrogen, as well as natural products that may influence interactions between microbes. Proteobacteria and Bacteroidetes members of the disease consortium are suited to the degradation of amino acids, proteins, and carbohydrates. The accumulation of sulfide underneath the black band mat, in part due to a lack of sulfur oxidizers, contributes to the lethality of the disease. The presence of sulfide:quinone oxidoreductase genes in all five Roseofilum MAGs and in the MAGs of several heterotrophs demonstrates that resistance to sulfide is an important characteristic for members of the BBD consortium.

Link between sewage-derived nitrogen pollution and coral disease severity in Guam.

The goals of this study were to evaluate the contribution of sewage-derived N to reef flat communities in Guam and to assess the impact of N inputs on coral disease. We used stable isotope analysis of macroalgae and a soft coral, sampled bimonthly, as a proxy for N dynamics, and surveyed Porites spp., a dominant coral taxon on Guam's reefs, for white syndrome disease severity. Results showed a strong influence of sewage-derived N in nearshore waters, with δ(15)N values varying as a function of species sampled, site, and sampling date. Increases in sewage-derived N correlated significantly with increases in the severity of disease among Porites spp., with δ(15)N values accounting for more than 48% of the variation in changes in disease severity. The anticipated military realignment and related population increase in Guam are expected to lead to increased white syndrome infections and other coral diseases.

Functionally diverse reef-fish communities ameliorate coral disease.

Coral reefs, the most diverse of marine ecosystems, currently experience unprecedented levels of degradation. Diseases are now recognized as a major cause of mortality in reef-forming corals and are complicit in phase shifts of reef ecosystems to algal-dominated states worldwide. Even so, factors contributing to disease occurrence, spread, and impact remain poorly understood. Ecosystem resilience has been linked to the conservation of functional diversity, whereas overfishing reduces functional diversity through cascading, top-down effects. Hence, we tested the hypothesis that reefs with trophically diverse reef fish communities have less coral disease than overfished reefs. We surveyed reefs across the central Philippines, including well-managed marine protected areas (MPAs), and found that disease prevalence was significantly negatively correlated with fish taxonomic diversity. Further, MPAs had significantly higher fish diversity and less disease than unprotected areas. We subsequently investigated potential links between coral disease and the trophic components of fish diversity, finding that only the density of coral-feeding chaetodontid butterflyfishes, seldom targeted by fishers, was positively associated with disease prevalence. These previously uncharacterized results are supported by a second large-scale dataset from the Great Barrier Reef. We hypothesize that members of the charismatic reef-fish family Chaetodontidae are major vectors of coral disease by virtue of their trophic specialization on hard corals and their ecological release in overfished areas, particularly outside MPAs.

Coral disease in Micronesian reefs: a link between disease prevalence and host abundance.

Current information regarding the effects of coral diseases on Indo-Pacific reefs lags behind that of the Caribbean. Considering that these reefs are geographically widespread, speciose, often highly influenced by human coastal populations, and inadequately monitored, developing a baseline database is a primary management issue for local scientists. In a first attempt to quantify diseases in Micronesia, Guam reefs were assessed for disease prevalence, host abundance, and community structure. Surveys of 15 reefs revealed 6 disease states affecting 8 families of reef-building corals and highly variable prevalence between sites, ranging from 0.2 to 12.6%. Guam reefs are taxonomically diverse but dominated by the genus Porites. Coral generic host abundance showed a significant and positive link with total disease prevalence. Five out of 6 of the observed disease states affected Porites spp. (mean prevalence within the genus: 6.14 +/- 0.88%), and acroporids and pocilloporids also showed high susceptibility. As the coral genera currently most affected by diseases are those providing the most structure to Guam's reefs, disease has the potential to have significant long-term effects, highlighting an urgent need for proactive management.

Coral diseases on Philippine reefs: genus Porites is a dominant host.

While it is generally assumed that Indo-Pacific reefs are not widely affected by diseases, limited data suggest a number of diseases and syndromes that appear to differ from those currently under study in the Caribbean. This report presents the results of a baseline survey of coral diseases in 2 regions in the Philippines: the Central Visayas and the Lingayen Gulf. Mean prevalence for all diseases observed was 8.3 +/- 1.2% (mean +/- SE; n = 8 reefs), with Central Visayas reefs showing higher disease prevalence (11.6 +/- 2.8%; n = 4 reefs) than those of Lingayen Gulf (5.1 +/- 1.4%; n = 4 reefs). Five diseases and syndromes were described; 3 of these-Porites ulcerative white spot disease (PUWS) (prevalence = 8.96 +/- 2.2%), tumors (prevalence = 1.0 +/- 0.5%) and pigmentation response (prevalence = 0.5 +/- 0.2%)--occurred frequently in both regions and targeted the genus Porites. Correlation between disease prevalence and number of Porites colonies was fairly strong (r2 = 43.4), though not significant, and no correlation was seen between prevalence and either the amount or diversity of hard coral. Porites is a major reef-builder in the Indo-Pacific comprising 30% of hard coral colonies on our surveyed reefs, and is generally thought to be a hardy, long-lived genus. Diseases targeting this robust group present an as yet unquantified risk to Philippine reefs and could result in major changes in reef structure.

Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease affecting Indo-Pacific reefs.

The results of an investigation of a new coral disease affecting Indo-Pacific reefs are presented. Porites ulcerative white spot disease (PUWS) is characterized by discrete, bleached, round foci, 3 to 5 mm in diameter, that may either regress or progress to full tissue-thickness ulcerations that coalesce, occasionally resulting in colony mortality. Monitoring of 25 diseased and 5 healthy reference colonies for 17 mo revealed that advanced stages of the disease were characterized by lesion coalescence, partial colony death (i.e. portions of the colony still alive; n = 17) and total colony death (n = 2). Field transmission experiments revealed that 95% of healthy colonies developed lesions within 5 wk after continual exposure to diseased branches, while 60% of the reference colonies remained healthy. The host range of PUWS includes branching and massive Porites spp., and prevalence per species was positively correlated with species density. On 10 reefs surveyed in the Central Philippines, 22 +/- 7% (mean +/- SE) of poritid colonies were infected, and the disease was present on 80% of the surveyed reefs. Poritids are dominant Indo-Pacific reef builders; a disease targeting this genus could cause major shifts in community structure over time. This report contributes to the limited knowledge of PUWS impacts in this region.