Machine-Learning-Based Proteomic Predictive Modeling with Thermally-Challenged Caribbean Reef Corals

Coral health is currently diagnosed retroactively; colonies are deemed “stressed” upon succumbing to bleaching or disease. Ideally, health inferences would instead be made on a pre-death timescale that would enable, for instance, environmental mitigation that could promote coral resilience. To this end, diverse Caribbean coral (Orbicella faveolata) genotypes of varying resilience to high temperatures along the Florida Reef Tract were exposed herein to elevated temperatures in the laboratory, and a proteomic analysis was taken with a subset of 20 samples via iTRAQ labeling followed by nano-liquid chromatography + mass spectrometry; 46 host coral and 40 Symbiodiniaceae dinoflagellate proteins passed all stringent quality control criteria, and the partial proteomes of biopsies of (1) healthy controls, (2) sub-lethally stressed samples, and (3) actively bleaching corals differed significantly from one another. The proteomic data were then used to train predictive models of coral colony bleaching susceptibility, and both generalized regression and machine-learning-based neural networks were capable of accurately forecasting the bleaching susceptibility of coral samples based on their protein signatures. Successful future testing of the predictive power of these models in situ could establish the capacity to proactively monitor coral health.

Ephemeral hypoxia reduces oxygen consumption in the Caribbean coral Orbicella faveolata

Oxygen concentrations in coastal waters have declined globally by 10% since the mid-twentieth century, and ocean warming will further reduce the solubility of oxygen in coastal habitats. Some nearshore reefs experience periodic hypoxic conditions due to eutrophication, especially during the wet season. Here, we determined the combined impacts of hypoxia and elevated temperature on the reef-building coral, Orbicella faveolata, by exposing corals to normoxic or hypoxic conditions and ambient or elevated temperatures. Oxygen consumption was monitored using closed-system respirometry. Corals within hypoxic conditions consumed 34% less oxygen relative to corals in normoxic conditions. Corals in the elevated temperature normoxic treatment experienced a 10% increase in oxygen consumption relative to the control. Corals exposed to both stressors simultaneously experienced a 62% reduction in oxygen consumption. These results suggest that increased temperature may exacerbate the negative effects of hypoxia on O. faveolata.

Measuring Stony Coral Tissue Loss Disease Induction and Lesion Progression Within Two Intermediately Susceptible Species, Montastraea cavernosa and Orbicella faveolata

During the last several decades, Florida’s Coral Reef (FCR) has been impacted by both global and local stressors that have devastated much of its living coral cover. Additionally, since 2014 FCR has experienced a lethal disease outbreak termed stony coral tissue loss disease (SCTLD). Here, we examined SCTLD spreading dynamics within and among fragmented coral colonies and quantified lesion progression rate of two intermediately susceptible species—Montastraea cavernosa and Orbicella faveolata—through induction experiments conducted in laboratory aquaria. M. cavernosa colonies showing subacute tissue loss were sequentially fragmented parallel to the lesion edge to determine whether isolated tissue that showed no tissue-loss signs, referred to as isolated apparently healthy (AH) donor fragments, would subsequently exhibit tissue loss. Additionally, AH M. cavernosa and O. faveolata fragments, referred to as recipient fragments, were placed in direct contact with the M. cavernosa donor fragments to assess incidence of new tissue-loss lesions. Finally, AH M. cavernosa donor fragments were placed in direct contact with recipient M. cavernosa and O. faveolata fragments to account for aggression from direct contact. Samples were collected for histopathology of the corals through time. Many isolated AH donor fragments developed tissue-loss lesions during the 60-day study, suggesting SCTLD may be systemic within small-sized colonies. Our results confirmed that physical contact between recipient fragments and subacute SCTLD-lesioned tissue often led to tissue loss in recipient fragments. None of the control recipient or donor fragments experienced tissue loss. Grossly, multifocal lesions started on or adjacent to the septal and costal basal body walls with tissue loss progressing across the polyp septa and coenenchyme, respectively, in both species. Histologically, initial tissue-loss lesions in both species exhibited characteristic lytic necrosis (LN) at the basal body wall of the gastrodermis. O. faveolata exhibited higher rates of lesion appearance and subsequent mortality compared to M. cavernosa, but once a lesion appeared, M. cavernosa lost tissue faster than O. faveolata. This work contributes to the growing knowledge of SCTLD dynamics and highlights the differences in lesion progression within susceptible species.

Physiological and ecological consequences of the water optical properties degradation on reef corals

Degradation of water optical properties due to anthropogenic disturbances is a common phenomenon in coastal waters globally. Although this condition is associated with multiple drivers that affect corals health in multiple ways, its effect on light availability and photosynthetic energy acquisition has been largely neglected. Here, we describe how declining the water optical quality in a coastal reef exposed to a turbid plume of water originating from a man-made channel compromises the functionality of the keystone coral species Orbicella faveolata. We found highly variable water optical conditions with significant effects on the light quantity and quality available for corals. Low-light phenotypes close to theoretical limits of photoacclimation were found at shallow depths as a result of reduced light penetration. The estimated photosynthetically fixed energy depletion with increasing depth was associated with patterns of colony mortality and vertical habitat compression. A numerical model illustrates the potential effect of the progressive water quality degradation on coral mortality and population decline along the depth gradient. Collectively, our findings suggest that preserving the water properties seeking to maximize light penetration through the water column is essential for maintaining the coral reef structure and associated ecosystem services.

Increasing coral calcification in Orbicella faveolata and Pseudodiploria strigosa at Flower Garden Banks, Gulf of Mexico

Coral reefs are globally in decline and western Atlantic reefs have experienced the greatest losses in live coral cover of any region. The Flower Garden Banks (FGB) in the Gulf of Mexico are high-latitude, remote reefs that are an outlier to this trend, as they have maintained coral cover ≥ 50% since at least 1989. Quantifying the long-term trends in coral growth of key reef-building coral species, and the underlying environmental drivers, leads to a better understanding of local sensitivities to past changes that will ultimately allow us to better predict the future of reef growth at FGB. We obtained coral cores and constructed growth records for two of the most abundant hermatypic coral species at FGB, Pseudodiploria strigosa and Orbicella faveolata. Our records cover 57 yrs of growth for P. strigosa (1957–2013) and 45 yrs for O. faveolata (1970–2014). Linear extension and calcification rates of both species have increased significantly, but skeletal density did not change over the respective time periods. Extension and calcification data of both species combined were negatively correlated with the discharge from the Atchafalaya River, but positively correlated with maximum sea surface temperatures (SST). These data provide evidence that runoff from the Atchafalaya River impacts FGB corals and is a major control on coral growth at FGB. The increase in growth at FGB can be attributed to the significant warming trend in maximum monthly SSTs. Given the warming trend and recent increase in severity of bleaching at FGB, the prognosis is that bleaching events will become more deleterious with time, which will lead to a breakdown in the positive relationship between coral growth and maximum SST. This study provides further evidence that some high-latitude, cooler reef sites have experienced a stimulation in coral growth with ocean warming.

Variation in susceptibility among three Caribbean coral species and their algal symbionts indicates the threatened staghorn coral, Acropora cervicornis, is particularly susceptible to elevated nutrients and heat stress

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal types were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N+P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (Fv/Fm) declines of 41-50%. In comparison, no mortality and lower Fv/Fm declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

Three-Dimensional Molecular Cartography of the Caribbean Reef-Building Coral Orbicella faveolata

All organisms host a diversity of associated viruses, bacteria, and protists, collectively defined as the holobiont. While scientific advancements have enhanced the understanding of the functional roles played by various components of the holobiont, there is a growing need to integrate multiple types of molecular data into spatially and temporally resolved frameworks. To that end, we mapped 16S and 18S rDNA metabarcoding, metatranscriptomics, and metabolomic data onto three-dimensional reconstructions of coral colonies to examine microbial diversity, microbial gene expression, and biochemistry on two colonies of the ecologically important, reef-building coral, Orbicella faveolata and their competitors (i.e., adjacent organisms interacting with the corals: fleshy algae, turf algae, hydrozoans, and other corals). Overall, no statistically significant spatial patterns were observed among the samples for any of the data types; instead, strong signatures of the macroorganismal hosts (e.g., coral, algae, hydrozoa) were detected, in the microbiome, the transcriptome, and the metabolome. The 16S rDNA analysis demonstrated higher abundance of Firmicutes in the coral microbiome than in its competitors. A single bacterial amplicon sequence variant from the genus Clostridium was found exclusively in all O. faveolata samples. In contrast to microbial taxa, a portion of the functionally annotated bacterial RNA transcripts (6.86%) and metabolites (1.95%) were ubiquitous in all coral and competitor samples. Machine learning analysis of microbial transcripts revealed elevated T7-like cyanophage-encoded photosystem II transcripts in O. faveolata samples, while sequences involved in bacterial cell division were elevated in turf algal and interface samples. Similar analysis of metabolites revealed that bacterial-produced antimicrobial and antifungal compounds were highly enriched in coral samples. This study provides insight into the spatial and biological patterning of the coral microbiome, transcriptome, and metabolome.

Physiological and ecological consequences of the water optical properties degradation on reef corals

Degradation of water optical properties due to anthropogenic disturbances is a common phenomenon in coastal waters globally. Although this condition is associated with multiple drivers that affect corals health in multiple ways, its effect on light availability and photosynthetic energy acquisition has been largely neglected. Here, we describe how declining the water optical quality in a coastal reef exposed to a turbid plume of water originating from a man-made channel compromise the functionality of the keystone coral species Orbicella faveolata. We found highly variable water optical conditions with significant effects on the light quantity and quality available for corals. Reduction of light penetration into the water column elicits the development of low-light phenotypes close to theoretical limits of photoacclimation despite their occurrence at shallow depths. Predicted photosynthetic energy depletion with increasing depth is associated with patterns of colony mortality and contraction of the habitable space for the population. A numerical model illustrates the potential effect the progressive degradation of water optical properties on the gradual mortality and population decline of O. faveolata. Our findings suggest that preserving the water optical properties seeking to maximize light penetration into the water column may have an extraordinary impact on coral reefs conservation, mostly toward the deeper portions of reefs.