Environmental Symbiont Acquisition May Not Be the Solution to Warming Seas for Reef-Building Corals

BACKGROUND: Coral reefs worldwide are in decline. Much of the mortality can be attributed to coral bleaching (loss of the coral's intracellular photosynthetic algal symbiont) associated with global warming. How corals will respond to increasing oceanic temperatures has been an area of extensive study and debate. Recovery after a bleaching event is dependent on regaining symbionts, but the source of repopulating symbionts is poorly understood. Possibilities include recovery from the proliferation of endogenous symbionts or recovery by uptake of exogenous stress-tolerant symbionts. METHODOLOGY/PRINCIPAL FINDINGS: To test one of these possibilities, the ability of corals to acquire exogenous symbionts, bleached colonies of Porites divaricata were exposed to symbiont types not normally found within this coral and symbiont acquisition was monitored. After three weeks exposure to exogenous symbionts, these novel symbionts were detected in some of the recovering corals, providing the first experimental evidence that scleractinian corals are capable of temporarily acquiring symbionts from the water column after bleaching. However, the acquisition was transient, indicating that the new symbioses were unstable. Only those symbiont types present before bleaching were stable upon recovery, demonstrating that recovery was from the resident in situ symbiont populations. CONCLUSIONS/SIGNIFICANCE: These findings suggest that some corals do not have the ability to adjust to climate warming by acquiring and maintaining exogenous, more stress-tolerant symbionts. This has serious ramifications for the success of coral reefs and surrounding ecosystems and suggests that unless actions are taken to reverse it, climate change will lead to decreases in biodiversity and a loss of coral reefs

Fine-scale morphological, genomic, reproductive, and symbiont differences delimit the Caribbean octocorals Plexaura homomalla and P. kükenthali

Octocorals are conspicuous members of coral reefs and deep-sea ecosystems. Yet, species boundaries and taxonomic relationships within this group remain poorly understood, hindering our understanding of this essential component of the marine fauna. We used a multifaceted approach to revisit the systematics of the Caribbean octocorals Plexaura homomalla and Plexaura kükenthali, two taxa that have a long history of taxonomic revisions. We integrated morphological and reproductive analyses with high-throughput sequencing technology to clarify the relationship between these common gorgonians. Although size and shape of the sclerites are significantly different, there is overlap in the distributions making identification based on sclerites alone difficult. Differences in reproductive timing and mode of larval development were detected, suggesting possible mechanisms of pre-zygotic isolation. Furthermore, there are substantial genetic differences and clear separation of the two species in nuclear introns and single-nucleotide polymorphisms obtained from de novo assembled transcriptomes. Despite these differences, analyses with SNPs suggest that hybridization is still possible between the two groups. The two nascent species also differed in their symbiont communities (genus Breviolum) across multiple sampling sites in the Caribbean. Despite a complicated history of taxonomic revisions, our results support the differentiation of P. homomalla and P. kükenthali, emphasizing that integrative approaches are essential for Anthozoan systematics

Tracking Transmission of Apicomplexan Symbionts in Diverse Caribbean Corals

Symbionts in each generation are transmitted to new host individuals either vertically (parent to offspring), horizontally (from exogenous sources), or a combination of both. Scleractinian corals make an excellent study system for understanding patterns of symbiont transmission since they harbor diverse symbionts and possess distinct reproductive modes of either internal brooding or external broadcast spawning that generally correlate with vertical or horizontal transmission, respectively. Here, we focused on the under-recognized, but apparently widespread, coral-associated apicomplexans (Protista: Alveolata) to determine if symbiont transmission depends on host reproductive mode. Specifically, a PCR-based assay was utilized towards identifying whether planula larvae and reproductive adults from brooding and broadcast spawning scleractinian coral species in Florida and Belize harbored apicomplexan DNA. Nearly all (85.5%; n = 85/89) examined planulae of five brooding species (Porites astreoides, Agaricia tenuifolia, Agaricia agaricites, Favia fragum, Mycetophyllia ferox) and adults of P. astreoides were positive for apicomplexan DNA. In contrast, no (n = 0/10) apicomplexan DNA was detected from planulae of four broadcast spawning species (Acropora cervicornis, Acropora palmata, Pseudodiploria strigosa, and Orbicella faveolata) and rarely in gametes (8.9%; n = 5/56) of these species sampled from the same geographical range as the brooding species. In contrast, tissue samples from nearly all (92.0%; n = 81/88) adults of the broadcast spawning species A. cervicornis, A. palmata and O. faveolata harbored apicomplexan DNA, including colonies whose gametes and planulae tested negative for these symbionts. Taken together, these data suggest apicomplexans are transmitted vertically in these brooding scleractinian coral species while the broadcast spawning scleractinian species examined here acquire these symbionts horizontally. Notably, these transmission patterns are consistent with those of other scleractinian coral symbionts. While this study furthers knowledge regarding these symbionts, numerous questions remain to be addressed, particularly in regard to the specific interaction(s) between these apicomplexans and their hosts

Coral life history and symbiosis: Functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata

<p>Abstract</p> <p>Background</p> <p>Scleractinian corals are the foundation of reef ecosystems in tropical marine environments. Their great success is due to interactions with endosymbiotic dinoflagellates (<it>Symbiodinium </it>spp.), with which they are obligately symbiotic. To develop a foundation for studying coral biology and coral symbiosis, we have constructed a set of cDNA libraries and generated and annotated ESTs from two species of corals, <it>Acropora palmata </it>and <it>Montastraea faveolata</it>.</p> <p>Results</p> <p>We generated 14,588 (<it>Ap</it>) and 3,854 (<it>Mf</it>) high quality ESTs from five life history/symbiosis stages (spawned eggs, early-stage planula larvae, late-stage planula larvae either infected with symbionts or uninfected, and adult coral). The ESTs assembled into a set of primarily stage-specific clusters, producing 4,980 (<it>Ap</it>), and 1,732 (<it>Mf</it>) unigenes. The egg stage library, relative to the other developmental stages, was enriched in genes functioning in cell division and proliferation, transcription, signal transduction, and regulation of protein function. Fifteen unigenes were identified as candidate symbiosis-related genes as they were expressed in all libraries constructed from the symbiotic stages and were absent from all of the non symbiotic stages. These include several DNA interacting proteins, and one highly expressed unigene (containing 17 cDNAs) with no significant protein-coding region. A significant number of unigenes (25) encode potential pattern recognition receptors (lectins, scavenger receptors, and others), as well as genes that may function in signaling pathways involved in innate immune responses (toll-like signaling, NFkB p105, and MAP kinases). Comparison between the <it>A. palmata </it>and an <it>A. millepora </it>EST dataset identified ferritin as a highly expressed gene in both datasets that appears to be undergoing adaptive evolution. Five unigenes appear to be restricted to the Scleractinia, as they had no homology to any sequences in the nr databases nor to the non-scleractinian cnidarians <it>Nematostella vectensis </it>and <it>Hydra magnipapillata</it>.</p> <p>Conclusion</p> <p>Partial sequencing of 5 cDNA libraries each for <it>A. palmata </it>and <it>M. faveolata </it>has produced a rich set of candidate genes (4,980 genes from <it>A. palmata</it>, and 1,732 genes from <it>M. faveolata</it>) that we can use as a starting point for examining the life history and symbiosis of these two species, as well as to further expand the dataset of cnidarian genes for comparative genomics and evolutionary studies.</p

Coral Reef Genomics: Developing tools for functional genomics ofcoral symbiosis

Symbioses between cnidarians and dinoflagellates in the genus Symbiodinium are widespread in the marine environment. The importance of this symbiosis to reef-building corals and reef nutrient and carbon cycles is well documented, but little is known about the mechanisms by which the partners establish and regulate the symbiosis. Because the dinoflagellate symbionts live inside the cells of their host coral, the interactions between the partners occur on cellular and molecular levels, as each partner alters the expression of genes and proteins to facilitate the partnership. These interactions can examined using high-throughput techniques that allow thousands of genes to be examined simultaneously. We are developing the groundwork so that we can use DNA microarray profiling to identify genes involved in the Montastraea faveolata and Acropora palmata symbioses. Here we report results from the initial steps in this microarray initiative, that is, the construction of cDNA libraries from 4 of 16 target stages, sequencing of 3450 cDNA clones to generate Expressed Sequenced Tags (ESTs), and annotation of the ESTs to identify candidate genes to include in the microarrays. An understanding of how the coral-dinoflagellate symbiosis is regulated will have implications for atmospheric and ocean sciences, conservation biology, the study and diagnosis of coral bleaching and disease, and comparative studies of animal-protest interactions

Macroalgal-Associated Dinoflagellates Belonging to the Genus Symbiodinium in Caribbean Reefs

Coral-algal symbiosis has been a subject of great attention during the last two decades in response to global coral reef decline. However, the occurrence and dispersion of free-living dinoflagellates belonging to the genus Symbiodinium are less documented. Here ecological and molecular evidence is presented demonstrating the existence of demersal free-living Symbiodinium populations in Caribbean reefs and the possible role of the stoplight parrotfish (Sparisoma viride) as Symbiodinium spp. dispersers. Communities of free-living Symbiodinium were found within macroalgal beds consisting of Halimeda spp., Lobophora variegata, Amphiroa spp., Caulerpa spp. and Dictyota spp. Viable Symbiodinium spp. cells were isolated and cultured from macroalgal beds and S. viride feces. Further identification of Symbiodinium spp. type was determined by length variation in the Internal Transcribed Spacer 2 (ITS2, nuclear rDNA) and length variation in domain V of the chloroplast large subunit ribosomal DNA (cp23S-rDNA). Determination of free-living Symbiodinium and mechanisms of dispersal is important in understanding the life cycle of Symbiodinium spp

Investigation and assimilation of nitrogen from benthic sediments by threee species of coral

We quantified the nitrogen and enzyme hydrolyzable amino acid (EHAA) concentrations of sediments prior to and after corals sloughed, ingested, and egested sediments layered onto their surfaces, for the three coral species Siderastrea siderea, Agaricia agaricites, and Porites astreoides in Jamaica. The percent nitrogen of the sediments egested by all three species was lower than in the sediments available to the corals. Additionally, the sediments sloughed (not ingested) by A. agaricites and P. astreoides were lower in percent nitrogen, while the sediments sloughed by S. siderea had the same percent nitrogen as that of the available sediments. The percent nitrogen of the sediments sloughed and egested by P. astreoides showed significant negative and positive relationships, respectively, to increasing sediment loads, while the percent nitrogen of the sediments sloughed and egested by both S. siderea and A. agaricites showed no relationship to sediment load. EHAA concentrations were not significantly different between the sloughed and available sediments but were significantly lower in the sediments egested by S. siderea and A. agaricites (EHAA concentrations were not measured for P. astreodies sediment fractions). Comparisons of the nitrogen and EHAA concentrations in the sloughed and egested sediments to what was available prior to coral processing show that maximum ingestion was between 0.1 and 0.2 µg N µg−1 coral N cm−2 and between 0.5 and 0.6 µg EHAA·cm−2. Maximum assimilation efficiencies were estimated to be 30–60% of the available nitrogen. The data show that corals ingest and alter the nitrogen concentration of particles that land on their surfaces. The corals’ abilities to process these sediments, and the sediments’ possible contributions to coral nutrition, are discussed based on these results

The Roles and Interactions of Symbiont, Host and Environment in Defining Coral Fitness

Background: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.\ud Methodology/Principal Findings: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31–35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.\ud Conclusions/Significance: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change

On the importance of the microbiome and pathobiome in coral health and disease

The term “microbiome” was first coined in 1988 and given the definition of a characteristic microbial community occupying a reasonably well defined habitat which has distinct physio-chemical properties. A more recent term has also emerged, taking this one step further and focusing on diseases in host organisms. The “pathobiome” breaks down the concept of “one pathogen = one disease” and highlights the role of the microbiome, more specifically certain members within the microbiome, in causing pathogenesis. The development of next generation sequencing has allowed large data sets to be amassed describing the microbial communities of many organisms and the field of coral biology is no exception. However, the choices made in the analytical process and the interpretation of these data can significantly affect the outcome and the overall conclusions drawn. In this review we explore the implications of these difficulties, as well as highlighting analytical tools developed in other research fields (such as network analysis) which hold substantial potential in helping to develop a deeper understanding of the role of the microbiome in disease in corals. We also make the case that standardization of methods will substantially improve the collective gain in knowledge across research groups.N/