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At least 19 records

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

The coral holobiont is comprised of a highly diverse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes, as it constitutes the direct interface between the coral host and the environment. Here, we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. The analysis was conducted using metagenomes and metagenome-assembled genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs. The microbial community structure in the coral SML varied according to the local environment, both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and those that are related to higher levels of microbial activity, competition, and stress response. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome, potentially increasing holobiont resilience to environmental changes and disease.

59 BASIC BIOLOGICAL SCIENCES↗

Coral mucus rapidly induces chemokinesis and genome-wide transcriptional shifts toward early pathogenesis in a bacterial coral pathogen

Elevated seawater temperatures have contributed to the rise of coral disease mediated by bacterial pathogens, such as the globally distributed Vibrio coralliilyticus, which utilizes coral mucus as a chemical cue to locate stressed corals. However, the physiological events in the pathogens that follow their entry into the coral host environment remain unknown. Here, we present simultaneous measurements of the behavioral and transcriptional responses of V. coralliilyticus BAA-450 incubated in coral mucus. Video microscopy revealed a strong and rapid chemokinetic behavioral response by the pathogen, characterized by a two-fold increase in average swimming speed within 6 min of coral mucus exposure. RNA sequencing showed that this bacterial behavior was accompanied by an equally rapid differential expression of 53% of the genes in the V. coralliilyticus genome. Specifically, transcript abundance 10 min after mucus exposure showed upregulation of genes involved in quorum sensing, biofilm formation, and nutrient metabolism, and downregulation of flagella synthesis and chemotaxis genes. After 60 min, we observed upregulation of genes associated with virulence, including zinc metalloproteases responsible for causing coral tissue damage and algal symbiont photoinactivation, and secretion systems that may export toxins. Together, our results suggest that V. coralliilyticus employs a suite of behavioral and transcriptional responses to rapidly shift into a distinct infection mode within minutes of exposure to the coral microenvironment.

54 ENVIRONMENTAL SCIENCES↗

Coral Gardens Reef, Belize: A refugium in the face of Caribbean-wide Acropora spp. coral decline

Caribbean Acropora spp. corals have undergone a decline in cover since the second half of the twentieth century. Loss of these architecturally complex and fast-growing corals has resulted in significant, cascading changes to the character, diversity, and available ecospaces of Caribbean reefs. Few thriving Acropora spp. populations exist today in the Caribbean and western North Atlantic seas, and our limited ability to access data from reefs assessed via long-term monitoring efforts means that reef scientists are challenged to determine resilience and longevity of existing Acropora spp. reefs. Here we used multiple dating methods to measure reef longevity and determine whether Coral Gardens Reef, Belize, is a refuge for Acropora cervicornis against the backdrop of wider Caribbean decline. We used a new genetic-aging technique to identify sample sites, and radiocarbon and high-precision uranium-thorium (U-Th) dating techniques to test whether one of the largest populations of extant A. cervicornis in the western Caribbean is newly established after the 1980s, or represents a longer-lived, stable population. We did so with respect for ethical sampling of a threatened species. Our data show corals ranging in age from 1910 ( 14 C) or 1915 ( 230 Th) to at least November 2019. While we cannot exclude the possibility of short gaps in the residence of A. cervicornis earlier in the record, the data show consistent and sustained living coral throughout the 1980s and up to at least 2019. We suggest that Coral Gardens has served as a refuge for A. cervicornis and that identifying other, similar sites may be critical to efforts to grow, preserve, conserve, and seed besieged Caribbean reefs.

58 GEOSCIENCES↗

Müllerian mimicry and the coloration patterns of sympatric coral snakes

Abstract Coral snakes in the genus Micrurus are venomous, aposematic organisms that signal danger to predators through vivid coloration. Previous studies found that they serve as models to several harmless species of Batesian mimics. However, the extent to which Micrurus species engage in Müllerian mimicry remains poorly understood. We integrate detailed morphological and geographical distribution data to investigate if coral snakes are Müllerian mimics. We found that coloration is spatially structured and that Micrurus species tend to be more similar where they co-occur. Though long supposed, we demonstrate for the first time that coral snakes might indeed be Müllerian mimics as they show some convergence in coloration patterns. Additionally, we found that the length of red-coloured rings in Micrurus is conserved, even at large geographic scales. This finding suggests that bright red rings may be under more substantial stabilizing selection than other aspects of coloration and probably function as a generalized signal for deterring predators.

Evolutionary Biology↗

CORAL Prototype Implementation (CORAL) v0.1

This is prototype code that implements many of the concepts in our invention, "The CORAL Framework for FAIR Data Management and Analysis" (ROI 2019-123, attached). The code includes a back end module that interfaces with third party open source software (ArangoDB), and a front end user interface (UI) that allows user interaction with the software through a web interface.

Chandonia, John-Marc↗

CORAL Prototype Implementation (CORAL) v0.1

This is prototype code that implements many of the concepts in our invention, "The CORAL Framework for FAIR Data Management and Analysis" (ROI 2019-123, attached). The code includes a back end module that interfaces with third party open source software (ArangoDB), and a front end user interface (UI) that allows user interaction with the software through a web interface.

Chandonia, John-Marc↗

Pre-Bleaching Coral Microbiome Is Enriched in Beneficial Taxa and Functions

Coral reef health is tightly connected to the coral holobiont, which is the association between the coral animal and a diverse microbiome functioning as a unit. The coral holobiont depends on key services such as nitrogen and sulfur cycling mediated by the associated bacteria. However, these microbial services may be impaired in response to environmental changes, such as thermal stress. A perturbed microbiome may lead to coral bleaching and disease outbreaks, which have caused an unprecedented loss in coral cover worldwide, particularly correlated to a warming ocean. The response mechanisms of the coral holobiont under high temperatures are not completely understood, but the associated microbial community is a potential source of acquired heat-tolerance. Here we investigate the effects of increased temperature on the taxonomic and functional profiles of coral surface mucous layer (SML) microbiomes in relationship to coral–algal physiology. We used shotgun metagenomics in an experimental setting to understand the dynamics of microbial taxa and genes in the SML microbiome of the coral Pseudodiploria strigosa under heat treatment. The metagenomes of corals exposed to heat showed high similarity at the level of bacterial genera and functional genes related to nitrogen and sulfur metabolism and stress response. The coral SML microbiome responded to heat with an increase in the relative abundance of taxa with probiotic potential, and functional genes for nitrogen and sulfur acquisition. Coral–algal physiology significantly explained the variation in the microbiome at taxonomic and functional levels. These consistent and specific microbial taxa and gene functions that significantly increased in proportional abundance in corals exposed to heat are potentially beneficial to coral health and thermal resistance.

59 BASIC BIOLOGICAL SCIENCES↗

Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network

Host-associated microbial communities are shaped by extrinsic and intrinsic factors to the holobiont organism. Environmental factors and microbe-microbe interactions act simultaneously on the microbial community structure, making the microbiome dynamics challenging to predict. The coral microbiome is essential to the health of coral reefs and sensitive to environmental changes. Here, we develop a dynamic model to determine the microbial community structure associated with the surface mucus layer (SML) of corals using temperature as an extrinsic factor and microbial network as an intrinsic factor. The model was validated by comparing the predicted relative abundances of microbial taxa to the relative abundances of microbial taxa from the sample data. The SML microbiome from Pseudodiploria strigosa was collected across reef zones in Bermuda, where inner and outer reefs are exposed to distinct thermal profiles. A shotgun metagenomics approach was used to describe the taxonomic composition and the microbial network of the coral SML microbiome. By simulating the annual temperature fluctuations at each reef zone, the model output is statistically identical to the observed data. The model was further applied to six scenarios that combined different profiles of temperature and microbial network to investigate the influence of each of these two factors on the model accuracy. The SML microbiome was best predicted by model scenarios with the temperature profile that was closest to the local thermal environment, regardless of the microbial network profile. Our model shows that the SML microbiome of P. strigosa in Bermuda is primarily structured by seasonal fluctuations in temperature at a reef scale, while the microbial network is a secondary driver. Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa. The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions.

59 BASIC BIOLOGICAL SCIENCES↗

Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

59 BASIC BIOLOGICAL SCIENCES↗

eCoral: How Electrolysis Could Restore Seawater Conditions Ideal for Coral Reefs

Coral reefs suffer from climate change, including long-term ocean acidification (OA) and warming and short-term bleaching, tropical storms, and pollution events, all of which are increasing in frequency and severity. It is urgent yet unclear how to intervene to save coral reefs. Reversal of the ocean pH to preindustrial levels could restore coral reefs to their preindustrial growth rates; however, strategies to reverse OA on environmentally relevant scales have not been established. Anecdotally, electrolysis seems to help coral reefs recover from acidification and short-term events, but few uncontrolled studies support such claims. Here, using two independent continuum simulation approaches (COMSOL and CrunchFlow), we show the effect of electrolysis on seawater chemistry relevant to coral reef survival and growth. We conclude that near the negative electrodes, the cathodes, seawater pH, supersaturation, and carbonate concentration all increase significantly. Electrolysis of seawater, therefore, can be used to restore preindustrial ocean conditions locally to save coral reefs, an approach termed eCoral here. We anticipate these simulation results to be the starting point for controlled experiments to test whether seawater electrolysis promotes coral reef growth and restoration, as these simulations predict.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

Fossil Corals With Various Degrees of Preservation Can Retain Information About Biomineralization-Related Organic Material

Scleractinian corals typically form a robust calcium carbonate skeleton beneath their living tissue. This skeleton, through its trace element composition and isotope ratios, may record environmental conditions of water surrounding the coral animal. While bulk unrecrystallized aragonite coral skeletons can be used to reconstruct past ocean conditions, corals that have undergone significant diagenesis have altered geochemical signatures and are typically assumed to retain insufficient meaningful information for bulk or macrostructural analysis. However, partially recrystallized skeletons may retain organic molecular components of the skeletal organic matrix (SOM), which is secreted by the animal and directs aspects of the biomineralization process. Some SOM proteins can be retained in fossil corals and can potentially provide past oceanographic, ecological, and indirect genetic information. Here, we describe a dataset of scleractinian coral skeletons, aged from modern to Cretaceous plus a Carboniferous rugosan, characterized for their crystallography, trace element composition, and amino acid compositions. We show that some specimens that are partially recrystallized to calcite yield potentially useful biochemical information whereas complete recrystalization or silicification leads to significant alteration or loss of the SOM fraction. Our analysis is informative to biochemical-paleoceanographers as it suggests that previously discounted partially recrystallized coral skeletons may indeed still be useful at the microstructural level.

58 GEOSCIENCES↗

Machine learning prediction of connectivity, biodiversity and resilience in the Coral Triangle

Abstract Even optimistic climate scenarios predict catastrophic consequences for coral reef ecosystems by 2100. Understanding how reef connectivity, biodiversity and resilience are shaped by climate variability would improve chances to establish sustainable management practices. In this regard, ecoregionalization and connectivity are pivotal to designating effective marine protected areas. Here, machine learning algorithms and physical intuition are applied to sea surface temperature anomaly data over a twenty-four-year period to extract ecoregions and assess connectivity and bleaching recovery potential in the Coral Triangle and surrounding oceans. Furthermore, the impacts of the El Niño Southern Oscillation (ENSO) on biodiversity and resilience are quantified. We find that resilience is higher for reefs north of the Equator and that the extraordinary biodiversity of the Coral Triangle is dynamic in time and space, and benefits from ENSO. The large-scale exchange of genetic material is enhanced between the Indian Ocean and the Coral Triangle during La Niña years, and between the Coral Triangle and the central Pacific in neutral conditions. Through machine learning the outstanding biodiversity of the Coral Triangle, its evolution and the increase of species richness are contextualized through geological times, while offering new hope for monitoring its future.

59 BASIC BIOLOGICAL SCIENCES↗

Identifying management opportunities to combat climate, land, and marine threats across less climate exposed coral reefs

Conserving coral reefs is critical for maintaining marine biodiversity, protecting coastlines, and supporting livelihoods in many coastal communities. Climate change threatens coral reefs globally, but researchers have identified a portfolio of coral reefs (bioclimatic units [BCUs]) that are relatively less exposed to climate impacts and strongly connected to other coral reef systems. These reefs provide a proactive opportunity to secure a long-term future for coral reefs under climate change. To help guide local management efforts, we quantified marine cumulative human impact (CHI) from climate, marine, and land pressures (2013 and from 2008 to 2013) in BCUs and across countries tasked with BCU management. Additionally, we created a management index based on common management measures and policies for each pressure source (climate, marine, and land) to identify a country's intent and commitment to effectively manage these pressures. Twenty-two countries (79%) had increases in CHI from 2008 to 2013. Climate change pressures had the highest proportional contribution to CHI across all reefs and in all but one country (Singapore), but 18 BCUs (35%) and nine countries containing BCUs (32%) had relatively high land and marine impacts. There was a significant positive relationship between climate impact and the climate management index across countries (R 2 = 0.43, p = 0.02), potentially signifying that countries with greater climate impacts are more committed to managing them. However, this trend was driven by climate management intent in Fiji and Bangladesh. Our results can be used to guide future fine-scale analyses, national policies, and local management decisions, and our management indices reveal areas where management components can be improved. Cost-effectively managing local pressures (e.g., fishing and nutrients) in BCUs is essential for building a climate-ready future that benefits coral reefs and people.

59 BASIC BIOLOGICAL SCIENCES↗

Investigating preservation of stable isotope ratios in subfossil deep-sea proteinaceous coral skeletons as paleo-recorders of biogeochemical information over multimillennial timescales

Paleoproxy records in deep-sea proteinaceous coral skeletons can reconstruct past ocean conditions on centennial to millennial time scales. Commonly recovered subfossil specimens could potentially extend these archives through the Holocene. However, protein matrix stability and integrity of stable isotope proxies over multi-millennial timescales in such specimens have never been examined. Here we compare amino acid (AA) composition together with bulk and AA compound-specific carbon (δ 13 C) and nitrogen (δ 15 N) isotopes in live-collected and subfossil (~9.6–11.6 kyrs BP) Kulamanamana haumeaae deep-sea coral specimens from the central Pacific to understand the effects of long-duration benthic oxic exposure on primary coral chemistry. We find large coupled shifts in bulk δ 15 N (~7‰) and δ 13 C (~2‰) in the outermost portion (0–10 mm) of the subfossil coral, coincident with extensive alteration of the protein matrix. Microstructural changes in skeletal texture coincide with higher C/N ratios (+0.8) and isotope-based amino acid degradation parameters (e.g. ΣV ≥ 3), indicating extensive degradation of seawater-exposed gorgonin. However, interior gorgonin (>10 mm) retained amino acid molecular compositions (with exception of major Glycine loss) and bulk and amino acid-specific isotopic values that were similar to live-collected specimens. These results indicate that compound-specific isotope analysis of amino acids can reconstruct paleo-oceanographic biogeochemical and ecosystem information in subfossil corals beyond a clear diagenetic horizon, which is easily identifiable from an evaluation of C/N ratios together with the ΣV degradation proxy.

58 GEOSCIENCES↗

Coral loss alters guarding and farming behavior of a Caribbean damselfish

Coral loss is a major element of global ecological change in the oceans that may shape the behavior of keystone species such as habitat-attached animals. Farming damselfishes cultivate and aggressively protect algal garden within their territory, thereby shaping local fish assemblages and macro-algae diversity. Following the widespread loss of live branching coral throughout Florida and the Caribbean Sea, dusky damselfish (Stegastes adustus) have modified their territorial behavior. We compared antagonistic behavior, and size and algal species composition of territories of dusky damselfish on dead branching coral rubble and live boulder coral in the Dry Tortugas National Park, USA. Even though similar numbers of “intruders” entered each habitat type, dusky damselfish on rubble territories chased out significantly more fishes, had larger territories and more species of algae were present in their gardens. This study shows that dusky damselfish successfully occupy living and dead coral areas; however, there are potential trade-offs between defending a larger territory and cultivating fewer algal species.

59 BASIC BIOLOGICAL SCIENCES↗

CORAL: A framework for rigorous self-validated data modeling and integrative, reproducible data analysis

Abstract Background Many organizations face challenges in managing and analyzing data, especially when relevant datasets arise from multiple sources and methods. Analyzing heterogeneous datasets and additional derived data requires rigorous tracking of their interrelationships and provenance. This task has long been a Grand Challenge of data science and has more recently been formalized in the FAIR principles: that all data objects be Findable, Accessible, Interoperable, and Reusable, both for machines and for people. Adherence to these principles is necessary for proper stewardship of information, for testing regulatory compliance, for measuring the efficiency of processes, and for facilitating reuse of data-analytical frameworks. Findings We present the Contextual Ontology-based Repository Analysis Library (CORAL), a platform that greatly facilitates adherence to all 4 of the FAIR principles, including the especially difficult challenge of making heterogeneous datasets Interoperable and Reusable across all parts of a large, long-lasting organization. To achieve this, CORAL's data model requires that data generators extensively document the context for all data, and our tools maintain that context throughout the entire analysis pipeline. CORAL also features a web interface for data generators to upload and explore data, as well as a Jupyter notebook interface for data analysts, both backed by a common API. Conclusions CORAL enables organizations to build FAIR data types on the fly as they are needed, avoiding the expense of bespoke data modeling. CORAL provides a uniquely powerful platform to enable integrative cross-dataset analyses, generating deeper insights than are possible using traditional analysis tools.

97 MATHEMATICS AND COMPUTING↗

From particle attachment to space-filling coral skeletons

Reef-building corals and their aragonite (CaCO 3 ) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ion-by-ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons’ resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling.

59 BASIC BIOLOGICAL SCIENCES↗