Christian R. Voolstra

The 2014-17 Global Coral Bleaching Event: The Most Severe and Widespread Coral Reef Destruction

Publisher: Research Square Platform LLC

Date: 06-06-2022

DOI: 10.21203/RS.3.RS-1555992/V1

Abstract: Ocean warming is increasing the incidence, scale, and severity of global-scale coral bleaching and mortality, culminating in the third global coral bleaching event that occurred during record marine heatwaves of 2014-2017. While local effects of these events have been widely reported, the global implications remain unknown. Analysis of 15,066 reef surveys during 2014-2017 revealed that 80% of surveyed reefs experienced significant coral bleaching and 35% experienced significant coral mortality. The global extent of significant coral bleaching and mortality was assessed by extrapolating results from reef surveys using comprehensive remote-sensing data of regional heat stress. This model predicted that 51% of the world’s coral reefs suffered significant bleaching and 15% significant mortality, surpassing damage from any prior global bleaching event. These observations demonstrate that global warming’s widespread damage to coral reefs is accelerating and underscores the threat anthropogenic climate change poses for the irreversible transformation of these essential ecosystems.

Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

Publisher: Cold Spring Harbor Laboratory

Date: 13-09-2017

DOI: 10.1101/188227

Abstract: Over the last century, the anthropogenic production of CO 2 has led to warmer (+0.74 °C) and more acidic (-0.1 pH) oceans 1 , resulting in increasingly frequent and severe mass bleaching events worldwide that precipitate global coral reef decline 2 , 3 . To mitigate this decline, proposals to augment the stress tolerance of corals through genetic and non-genetic means have been gaining traction 4 . Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization 5,6 . While DNA methylation has been observed in corals 7-10 , its potential role in phenotypic plasticity has not yet been described. Here, we show that, similar to findings in mice 11 , DNA methylation significantly reduces spurious transcription in the Red Sea coral Stylophora pistillata , suggesting the evolutionary conservation of this essential mechanism in corals. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the maintenance of linear extension rates under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization, providing corals with an additional mechanism to cope with climate change.

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

Publisher: MDPI AG

Date: 21-06-2022

DOI: 10.20944/PREPRINTS202206.0284.V1

Abstract: Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine ersity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellies), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic ersity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic ersity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Insights into the cultured bacterial fraction of corals

Publisher: Research Square Platform LLC

Date: 21-11-2020

DOI: 10.21203/RS.3.RS-105866/V1

Abstract: Bacteria associated with coral hosts are erse and abundant, with recent studies suggesting involvement of these symbionts in host resilience to anthropogenic stress. Despite the putative importance of bacteria, the work dedicated to culturing coral-associated bacteria has received little attention. Combining published and unpublished data, here we report a comprehensive overview of the ersity and function of culturable, coral-associated bacteria. A total of 3055 isolates from 52 studies were considered by our meta-survey. Of these, 1045 had full length 16S rRNA gene sequences, spanning 138 formally described and 12 putatively novel bacterial genera across the Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria phyla. We performed comparative genomic analysis using the available genomes of 74 strains and identified potential signatures of beneficial bacterial-coral symbioses among them. Our analysis revealed biosynthetic gene clusters that underlie the biosynthesis of antioxidant, antimicrobial, cytotoxic, and other secondary metabolites. Moreover, we uncovered genomic features - not previously described for coral-bacterial symbioses - involved in host colonization and host-symbiont recognition, antiviral defence mechanisms, and/or integrated metabolic interactions, which we suggest as novel targets for the screening of coral probiotics. Our results highlight the importance of bacterial cultures to elucidate coral holobiont functioning, and guide the selection of probiotic candidates to promote coral resilience and improve reef restoration efforts.

Comparative genomics explains the evolutionary success of reef-forming corals

Publisher: eLife Sciences Publications, Ltd

Date: 24-05-2016

DOI: 10.7554/ELIFE.13288

Abstract: Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.

Aiptasia as a model to study metabolic diversity and specificity in cnidarian-dinoflagellate symbioses

Publisher: Cold Spring Harbor Laboratory

Date: 22-11-2017

DOI: 10.1101/223933

Abstract: The symbiosis between cnidarian hosts and microalgae of the genus Symbiodinium provides the foundation of coral reefs in oligotrophic waters. Understanding the nutrient-exchange between these partners is key to identifying the fundamental mechanisms behind this symbiosis. However, deciphering the in idual role of host and algal partners in the uptake and cycling of nutrients has proven difficult, given the endosymbiotic nature of this relationship. In this study, we highlight the advantages of the emerging model system Aiptasia to investigate the metabolic ersity and specificity of cnidarian – dinoflagellate symbiosis. For this, we combined traditional measurements with nano-scale secondary ion mass spectrometry (NanoSIMS) and stable isotope labeling to investigate carbon and nitrogen cycling both at the organismal scale and the cellular scale. Our results suggest that the in idual nutrient assimilation by hosts and symbionts depends on the identity of their respective symbiotic partner. Further, δ 13 C enrichment patterns revealed that alterations in carbon fixation rates only affected carbon assimilation in the cnidarian host but not the algal symbiont, suggesting a ‘selfish’ character of this symbiotic association. Based on our findings, we identify new venues for future research regarding the role and regulation of nutrient exchange in the cnidarian - dinoflagellate symbiosis. In this context, the model system approach outlined in this study constitutes a powerful tool set to address these questions.

Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

Publisher: American Association for the Advancement of Science (AAAS)

Date: 06-2018

DOI: 10.1126/SCIADV.AAR8028

Abstract: Changes in gene body methylation predict phenotypic acclimatization of the coral Stylophora pistillata to ocean acidification.

Heat stress destabilizes symbiotic nutrient cycling in corals

Publisher: Proceedings of the National Academy of Sciences

Date: 26-01-2021

DOI: 10.1073/PNAS.2022653118

Abstract: Ocean warming is causing repeated mass coral bleaching, leading to catastrophic losses of coral reefs worldwide. Our ability to slow or revert this decline is h ered by an incomplete understanding of the processes underlying the breakdown of the coral–algal symbiosis. Here, we show that heat stress destabilizes the nutrient cycling between corals and their endosymbiotic algae long before bleaching becomes apparent. Notably, increased metabolic energy demands shift the coral–algal symbiosis from a nitrogen- to a carbon-limited state, reducing translocation and recycling of photosynthetic carbon. This effectively undermines the ecological advantage of harboring algal symbionts and directly contributes to the breakdown of the coral–algal symbiosis during heat stress.

Hypoxia as a physiological cue and pathological stress for coral larvae

Publisher: Wiley

Date: 14-11-2021

DOI: 10.1111/MEC.16259

Abstract: Ocean deoxygenation events are intensifying worldwide and can rapidly drive adult corals into a state of metabolic crisis and bleaching‐induced mortality, but whether coral larvae are subject to similar stress remains untested. We experimentally exposed apo‐symbiotic coral larvae of Acropora selago to deoxygenation stress with subsequent reoxygenation aligned to their night‐day light cycle, and followed their gene expression using RNA‐Seq. After 12 h of deoxygenation stress (~2 mg O 2 /L), coral planulae demonstrated a low expression of HIF‐targeted hypoxia response genes concomitant with a significantly high expression of PHD2 (a promoter of HIFα proteasomal degradation), similar to corresponding adult corals. Despite exhibiting a consistent swimming phenotype compared to control s les, the differential gene expression observed in planulae exposed to deoxygenation‐reoxygenation suggests a disruption of pathways involved in developmental regulation, mitochondrial activity, lipid metabolism, and O 2 ‐sensitive epigenetic regulators. Importantly, we found that treated larvae exhibited a disruption in the expression of conserved HIF‐targeted developmental regulators, for ex le, Homeobox ( HOX ) genes, corroborating how changes in external oxygen levels can affect animal development. We discuss how the observed deoxygenation responses may be indicative of a possible acclimation response or alternatively may imply negative latent impacts for coral larval fitness.

Harnessing the microbiome to prevent global biodiversity loss.

Publisher: Springer Science and Business Media LLC

Date: 21-07-2022

DOI: 10.1038/S41564-022-01173-1

Abstract: Global bio ersity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of bio ersity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.

Integrating environmental variability to broaden the research on coral responses to future ocean conditions

Publisher: Wiley

Date: 03-09-2021

DOI: 10.1111/GCB.15840

Abstract: Our understanding of the response of reef‐building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long‐term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in‐situ seasonal and diurnal variability of key environmental drivers (temperature, p CO 2 , and O 2 ) critical for the growth and livelihood of reef‐building corals. Using a meta‐analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short‐term hourly fluctuations of temperature and p CO 2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, p CO 2 , and dissolved O 2 , which warrants site‐specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O 2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.

Human‐induced salinity changes impact marine organisms and ecosystems

Publisher: Wiley

Date: 12-07-2023

DOI: 10.1111/GCB.16859

Abstract: Climate change is fundamentally altering marine and coastal ecosystems on a global scale. While the effects of ocean warming and acidification on ecology and ecosystem functions and services are being comprehensively researched, less attention is directed toward understanding the impacts of human‐driven ocean salinity changes. The global water cycle operates through water fluxes expressed as precipitation, evaporation, and freshwater runoff from land. Changes to these in turn modulate ocean salinity and shape the marine and coastal environment by affecting ocean currents, stratification, oxygen saturation, and sea level rise. Besides the direct impact on ocean physical processes, salinity changes impact ocean biological functions with the ecophysiological consequences are being poorly understood. This is surprising as salinity changes may impact ersity, ecosystem and habitat structure loss, and community shifts including trophic cascades. Climate model future projections (of end of the century salinity changes) indicate magnitudes that lead to modification of open ocean plankton community structure and habitat suitability of coral reef communities. Such salinity changes are also capable of affecting the ersity and metabolic capacity of coastal microorganisms and impairing the photosynthetic capacity of (coastal and open ocean) phytoplankton, macroalgae, and seagrass, with downstream ramifications on global biogeochemical cycling. The scarcity of comprehensive salinity data in dynamic coastal regions warrants additional attention. Such datasets are crucial to quantify salinity‐based ecosystem function relationships and project such changes that ultimately link into carbon sequestration and freshwater as well as food availability to human populations around the globe. It is critical to integrate vigorous high‐quality salinity data with interacting key environmental parameters (e.g., temperature, nutrients, oxygen) for a comprehensive understanding of anthropogenically induced marine changes and its impact on human health and the global economy.

Condition-specific RNA editing in the coral symbiont Symbiodinium microadriaticum

Publisher: Public Library of Science (PLoS)

Date: 28-02-2017

DOI: 10.1371/JOURNAL.PGEN.1006619

Evidence for miRNA‐mediated modulation of the host transcriptome in cnidarian–dinoflagellate symbiosis

Publisher: Wiley

Date: 23-12-2017

DOI: 10.1111/MEC.14452

Abstract: Reef-building corals and other cnidarians living in symbiotic relationships with intracellular, photosynthetic dinoflagellates in the genus Symbiodinium undergo transcriptomic changes during infection with the algae and maintenance of the endosymbiont population. However, the precise regulatory mechanisms modulating the host transcriptome are unknown. Here, we report apparent post-transcriptional gene regulation by miRNAs in the sea anemone Aiptasia, a model system for cnidarian-dinoflagellate endosymbiosis. Aiptasia encodes mainly species-specific miRNAs, and there appears to have been recent differentiation within the Aiptasia genome of miRNAs that are commonly conserved among anthozoan cnidarians. Analysis of miRNA expression showed that both conserved and species-specific miRNAs are differentially expressed in response to endosymbiont infection. Using cross-linking immunoprecipitation of Argonaute, the central protein of the miRNA-induced silencing complex, we identified miRNA binding sites on a transcriptome-wide scale and found that the targets of the miRNAs regulated in response to symbiosis include genes previously implicated in biological processes related to Symbiodinium infection. Our study shows that cnidarian miRNAs recognize their mRNA targets via high-complementarity target binding and suggests that miRNA-mediated modulations of genes and pathways are important during the onset and maintenance of cnidarian-dinoflagellate endosymbiosis.

Desert plant bacteria reveal host influence and beneficial plant growth properties

Publisher: Public Library of Science (PLoS)

Date: 12-12-2018

DOI: 10.1371/JOURNAL.PONE.0208223

Publisher Correction: Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

Publisher: Springer Science and Business Media LLC

Date: 23-08-2018

DOI: 10.1038/S42003-018-0117-4

Abstract: In the original HTML version of the paper, the following affiliation was missing for author Cheong Xin Chan: School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia. This affiliation was incorrectly assigned to author Pim Bongaerts as “Present Address”. All affiliations were published correctly in the PDF version of the paper and have now been corrected in the HTML.

Symbiodinium genomes reveal adaptive evolution of functions related to symbiosis

Publisher: Cold Spring Harbor Laboratory

Date: 05-10-2017

DOI: 10.1101/198762

Abstract: Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the world’s coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp), previously sequenced as strain CCMP2468, to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identified extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding Symbiodinium biology and the coral-algal symbiosis.

Probiotics reshape the coral microbiome in situ without affecting the surrounding environment

Publisher: Research Square Platform LLC

Date: 31-10-2023

DOI: 10.21203/RS.3.RS-3414265/V1

Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

Publisher: Elsevier BV

Date: 04-2019

DOI: 10.1016/J.ZOOL.2019.02.007

Abstract: Current research highlights the importance of associated microbes in contributing to the functioning, health, and even adaptation of their animal, plant, and fungal hosts. As such, we are witnessing a shift in research that moves away from focusing on the eukaryotic host sensu stricto to research into the complex conglomerate of the host and its associated microorganisms (i.e., microbial eukaryotes, archaea, bacteria, and viruses), the so-called metaorganism, as the biological entity. While recent research supports and encourages the adoption of such an integrative view, it must be understood that microorganisms are not involved in all host processes and not all associated microorganisms are functionally important. As such, our intention here is to provide a critical review and evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework and the functional toolbox available to do so. We note that marker gene-guided approaches that primarily characterize microbial ersity are a first step in delineating associated microbes but are not sufficient to establish proof of their functional relevance. More sophisticated tools and experiments are necessary to reveal the specific functions of associated microbes. This can be accomplished through the study of metaorganisms in less complex environments, the targeted manipulation of microbial associates, or work at the mechanistic level with the toolbox available in model systems. We conclude that the metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions such as the evolution and ecology of organismal complexity and the importance of organismal symbioses to ecosystem functioning. The intricacy of the metaorganism requires a holistic framework combining reductionist and integrative approaches to resolve the structure and function of its member species and to disclose the various roles that microorganisms play in the biology of their hosts.

Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

Publisher: Wiley

Date: 17-01-2019

DOI: 10.1002/ECE3.4662

A genomic view of the reef-building coral Porites lutea and its microbial symbionts

Publisher: Springer Science and Business Media LLC

Date: 23-09-2019

DOI: 10.1038/S41564-019-0532-4

Abstract: Corals and the reef ecosystems that they support are in global decline due to increasing anthropogenic pressures such as climate change

High summer temperatures amplify functional differences between coral‐ and algae‐dominated reef communities

Publisher: Wiley

Date: 27-12-2020

DOI: 10.1002/ECY.3226

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Publisher: Springer Science and Business Media LLC

Date: 02-12-2021

DOI: 10.1038/S41396-021-01158-8

Abstract: Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph ersity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.

Long-Term Impacts of the 1997–1998 Bleaching Event on the Growth and Resilience of Massive Porites Corals From the Central Red Sea

Publisher: American Geophysical Union (AGU)

Date: 06-2019

DOI: 10.1029/2019GC008312

Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia

Publisher: American Association for the Advancement of Science (AAAS)

Date: 17-03-2023

DOI: 10.1126/SCIADV.ADF7108

Abstract: Symbiotic cnidarians such as corals and anemones form highly productive and bio erse coral reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwin’s paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated up-regulation and relocalization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through glutamine synthetase/glutamate synthase–mediated amino acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments.

Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

Publisher: Springer Science and Business Media LLC

Date: 14-12-2017

DOI: 10.1038/S41598-017-17484-X

Abstract: Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary ergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata , and compared it to the available genome of a complex coral, Acropora digitifera . We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals erged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.

Microbes support enhanced nitrogen requirements of coral holobionts in a high CO₂ environment

Publisher: Wiley

Date: 04-10-2021

DOI: 10.1111/MEC.16163

Abstract: Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO 2 conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfil their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO 2 seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO 2 conditions. Our results demonstrate for the first time that under high p CO 2 conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph‐derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO 2 control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha‐proteobacterium. Further, corals at the high CO 2 site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N‐rich picoplankton sources to offset their increased N requirements may be able to cope better in a high p CO 2 world.

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

Publisher: American Association for the Advancement of Science (AAAS)

Date: 03-08-2018

DOI: 10.1126/SCIADV.AAT2142

Abstract: The epigenetic mechanism of DNA methylation optimizes gene expression in endosymbiosis between cnidarians and their microalgae.

Flexibility in Red Sea Tridacna maxima‐Symbiodiniaceae associations supports environmental niche adaptation

Publisher: Wiley

Date: 11-03-2021

DOI: 10.1002/ECE3.7299

Abstract: Giant clams (Tridacninae) are important members of Indo‐Pacific coral reefs and among the few bivalve groups that live in symbiosis with unicellular algae (Symbiodiniaceae). Despite the importance of these endosymbiotic dinoflagellates for clam ecology, the ersity and specificity of these associations remain relatively poorly studied, especially in the Red Sea. Here, we used the internal transcribed spacer 2 (ITS2) rDNA gene region to investigate Symbiodiniaceae communities associated with Red Sea Tridacna maxima clams. We s led five sites spanning 1,300 km (10° of latitude, from the Gulf of Aqaba, 29°N, to the Farasan Banks, 18°N) along the Red Sea's North‐South environmental gradient. We detected a erse and structured assembly of host‐associated algae with communities demonstrating region and site‐specificity. Specimens from the Gulf of Aqaba harbored three genera of Symbiodiniaceae, Cladocopium, Durusdinium , and Symbiodinium , while at all other sites clams associated exclusively with algae from the Symbiodinium genus. Of these exclusively Symbiodinium ‐associating sites, the more northern (27° and 22°) and more southern sites (20° and 18°) formed two separate groupings despite site‐specific algal genotypes being resolved at each site. These groupings were congruent with the genetic break seen across multiple marine taxa in the Red Sea at approximately 19°, and along with our documented site‐specificity of algal communities, contrasted the panmictic distribution of the T. maxima host. As such, our findings indicate flexibility in T. maxima ‐Symbiodiniaceae associations that may explain its relatively high environmental plasticity and offers a mechanism for environmental niche adaptation.

Low Symbiodiniaceae diversity in a turbid marginal reef environment

Publisher: Springer Science and Business Media LLC

Date: 06-2020

DOI: 10.1007/S00338-020-01956-0

High Summer Temperatures Amplify Functional Differences Between Coral‐ and Algae‐Dominated Reef Communities

Publisher: Wiley

Date: 2021

DOI: 10.1002/BES2.1822

Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment

Publisher: Springer Science and Business Media LLC

Date: 03-02-2020

DOI: 10.1007/S00338-019-01889-3

Environmental latitudinal gradients and host‐specificity shape Symbiodiniaceae distribution in Red Sea Porites corals

Publisher: Wiley

Date: 13-08-2019

DOI: 10.1111/JBI.13672

Divergent expression of hypoxia response systems under deoxygenation in reef‐forming corals aligns with bleaching susceptibility

Publisher: Wiley

Date: 16-11-2020

DOI: 10.1111/GCB.15436

Rebuilding Coral Reefs: A Decadal Grand Challenge

Publisher: International Coral Reef Society and Future Earth Coasts

Date: 20-07-2021

DOI: 10.53642/NRKY9386

Abstract: This document is the work of a team assembled by the International Coral Reef Society (ICRS). The mission of ICRS is to promote the acquisition and dissemination of scientific knowledge to secure the future of coral reefs, including via relevant policy frameworks and decision-making processes. This document seeks to highlight the urgency of taking action to conserve and restore reefs through protection and management measures, to provide a summary of the most relevant and recent natural and social science that provides guidance on these tasks, and to highlight implications of these findings for the numerous discussions and negotiations taking place at the global level.

Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility

Publisher: Springer Science and Business Media LLC

Date: 15-07-2022

DOI: 10.1038/S41396-022-01283-Y

Abstract: The skeleton of reef-building coral harbors erse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic ersity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea , two common reef‐building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15 N and 13 C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional ersity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea . We propose that the lower endolithic primary productivity in G . edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral modelAiptasia

Publisher: Cold Spring Harbor Laboratory

Date: 02-11-2017

DOI: 10.1101/213066

Abstract: The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research is focusing on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, which have been implicated in transcriptional regulation and acclimation to environmental change, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia . We find methylated genes are marked by histone H3K36me3 and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes such as immunity, apoptosis, phagocytosis recognition and phagosome formation, and unveil intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis during symbiosis.

Rapid adaptive responses to climate change in corals

Publisher: Springer Science and Business Media LLC

Date: 09-2017

DOI: 10.1038/NCLIMATE3374

Fishery biomass trends of exploited fish populations in marine ecoregions, climatic zones and ocean basins

Publisher: Elsevier BV

Date: 09-2020

DOI: 10.1016/J.ECSS.2020.106896

Coral reef survival under accelerating ocean deoxygenation

Publisher: Springer Science and Business Media LLC

Date: 31-03-2020

DOI: 10.1038/S41558-020-0737-9

Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations

Publisher: Springer Science and Business Media LLC

Date: 16-03-2020

DOI: 10.1007/S00338-020-01917-7

Abstract: Widespread coral bleaching occurred in the central Red Sea in 2010 and 2015. During both events, a cross-shelf and depth gradient of bleaching severity was identified within the Thuwal reef system, central Red Sea, Saudi Arabia. While bleaching and survival of coral taxa were monitored, neither in situ reef temperatures nor coral-associated algal communities (family Symbiodiniaceae) were characterized. Here, we determined coral host-associated Symbiodiniaceae communities and monitored temperatures along the same cross-shelf and depth gradient on six reefs in 2017 to better understand the role of these factors in the observed bleaching patterns and to generate a baseline for further studies. We characterized 600 coral–algal associations across winter and summer in six genera of scleractinian coral ( Pocillopora, Stylophora, Seriatopora, Galaxea, Gardineroseris, and Porites ) and one fire coral (Family Milleporidae) using ITS2 next-generation sequencing in conjunction with the SymPortal analytical framework. We show that previous bleaching patterns correlate poorly with the largely coral host-specific structure of the 2017 Symbiodiniaceae community and are in better agreement with absolute and intraday sea water temperature variations monitored on the reefs. We demonstrate a greater distinctiveness of Symbiodiniaceae communities at the more severely bleached inshore reefs compared to those reefs further offshore. However, the potential Symbiodiniaceae community changes at these reefs prior to our s ling prevent us from evaluating this distinctiveness as determinative of the differences in bleaching severities. Based on our analyses, we discuss how fine-scale delineation of algal genotypes, including host-specific putative genotypes of Durusdinium trenchii that represent alluring targets for further taxonomic identification, corroborate a niche-adapted rather than generalist character of many coral–Symbiodiniaceae associations. In conclusion, as studies such as this one continue to build the global catalogue of coral–Symbiodiniaceae associations, we may be afforded a better oversight of how specialized coral–algal associations really are and how restricted their modification may be, both of which are critical considerations in predicting the adaptive potential of corals and the reef ecosystems they build.

Association of coral algal symbionts with a diverse viral community responsive to heat shock

Publisher: Springer Science and Business Media LLC

Date: 17-08-2017

DOI: 10.1186/S12866-017-1084-5

Increasing comparability among coral bleaching experiments

Publisher: Wiley

Date: 04-05-2021

DOI: 10.1002/EAP.2262

Abstract: Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the erse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For ex le, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross‐study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide.

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Publisher: PeerJ

Date: 02-05-2023

DOI: 10.7717/PEERJ.15023

Abstract: Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine ersity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians ( e.g ., corals, octocorals, sea anemones, jellyfish), other marine invertebrates ( e.g. , sponges, molluscs, flatworms), and protists ( e.g ., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic ersity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic ersity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Coral-bleaching responses to climate change across biological scales.

Publisher: Wiley

Date: 27-04-2022

DOI: 10.1111/GCB.16192

Abstract: The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for ex le hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km

Transcriptomes and expression profiling of deep-sea corals from the Red Sea provide insight into the biology of azooxanthellate corals

Publisher: Springer Science and Business Media LLC

Date: 25-07-2017

DOI: 10.1038/S41598-017-05572-X

Abstract: Despite the importance of deep-sea corals, our current understanding of their ecology and evolution is limited due to difficulties in s ling and studying deep-sea environments. Moreover, a recent re-evaluation of habitat limitations has been suggested after characterization of deep-sea corals in the Red Sea, where they live at temperatures of above 20 °C at low oxygen concentrations. To gain further insight into the biology of deep-sea corals, we produced reference transcriptomes and studied gene expression of three deep-sea coral species from the Red Sea, i.e. Dendrophyllia sp., Eguchipsammia fistula , and Rhizotrochus typus . Our analyses suggest that deep-sea coral employ mitochondrial hypometabolism and anaerobic glycolysis to manage low oxygen conditions present in the Red Sea. Notably, we found expression of genes related to surface cilia motion that presumably enhance small particle transport rates in the oligotrophic deep-sea environment. This is the first study to characterize transcriptomes and in situ gene expression for deep-sea corals. Our work offers several mechanisms by which deep-sea corals might cope with the distinct environmental conditions present in the Red Sea As such, our data provide direction for future research and further insight to organismal response of deep-sea coral to environmental change and ocean warming.

Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities

Publisher: Springer Science and Business Media LLC

Date: 06-02-2020

DOI: 10.1186/S40168-019-0776-5

Abstract: The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience to future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) is a potential mechanism that may assist corals to thrive in warm waters. The northern Red Sea experiences extreme temperatures anomalies, yet corals in this area rarely bleach suggesting possible refugia to climate change. However, the coral microbiome composition, and how it relates to the capacity to thrive in warm waters in this region, is entirely unknown. We investigated microbiomes for six coral species ( Porites nodifera, Favia favus, Pocillopora damicornis , Seriatopora hystrix , Xenia umbellata , and Sarcophyton trocheliophorum ) from five sites in the northern Red Sea spanning 4° of latitude and summer mean temperature ranges from 26.6 °C to 29.3 °C. A total of 19 distinct dinoflagellate endosymbionts were identified as belonging to three genera in the family Symbiodiniaceae ( Symbiodinium , Cladocopium , and Durusdinium ). Of these, 86% belonged to the genus Cladocopium , with notably five novel types (19%). The endosymbiont community showed a high degree of host-specificity despite the latitudinal gradient. In contrast, the ersity and composition of bacterial communities of the surface mucus layer (SML)—a compartment particularly sensitive to environmental change—varied significantly between sites, however for any given coral was species-specific. The conserved endosymbiotic community suggests high physiological plasticity to support holobiont productivity across the different latitudinal regimes. Further, the presence of five novel algal endosymbionts suggests selection of certain genotypes (or genetic adaptation) within the semi-isolated Red Sea. In contrast, the dynamic composition of bacteria associated with the SML across sites may contribute to holobiont function and broaden the ecological niche. In doing so, SML bacterial communities may aid holobiont local acclimatization (or adaptation) by readily responding to changes in the host environment. Our study provides novel insight about the selective and endemic nature of coral microbiomes along the northern Red Sea refugia.

Extending the natural adaptive capacity of coral holobionts

Publisher: Springer Science and Business Media LLC

Date: 12-10-2021

DOI: 10.1038/S43017-021-00214-3

King Abdullah University Of Sience And Technology

Location: Saudi Arabia

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King Abdullah University Of Science And Technology

Location: Saudi Arabia

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University Of Konstanz

Location: Germany

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University Of Cologne

Location: Germany

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University Of California Merced

Location: United States of America

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Discovery Projects - Grant ID: DP230100210

Start Date: 09-2023

End Date: 08-2026

Amount: $611,798.00

Funder: Australian Research Council

Discovery Projects - Grant ID: DP180100074

Start Date: 2018

End Date: 12-2020

Amount: $421,580.00

Funder: Australian Research Council