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

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/

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 Adaptive Bleaching Hypothesis: Experimental Tests of Critical Assumptions

Coral bleaching, the loss of color due to loss of symbiotic zooxanthellae or their pigment, appears to be increasing in intensity and geographic extent, perhaps related to increasing sea surface temperatures. The adaptive bleaching hypothesis (ABH) posits that when environmental circumstances change, the loss of one or more kinds of zooxanthellae is rapidly, sometimes unnoticeably, followed by formation of a new symbiotic consortium with different zooxanthellae that are more suited to the new conditions in the host's habitat. Fundamental assumptions of the ABH include (1) different types of zooxanthellae respond differently to environmental conditions, specifically temperature, and (2) bleached adults can secondarily acquire zooxanthellae from the environment. We present simple tests of these assumptions and show that (1) genetically different strains of zooxanthellae exhibit different responses to elevated temperature, (2) bleached adult hosts can acquire algal symbionts with an apparently dose-dependent relationship between the concentration of zooxanthellae and the rate of establishment of the symbiosis, (3) and finally, bleached adult hosts can acquire symbionts from the water column.PublishedYe

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

Productivity links morphology, symbiont specificity, and bleaching in the evolution of Caribbean octocoral symbioses

Many cnidarians host endosymbiotic dinoflagellates from the genus Symbiodinium. It is generally assumed that the symbiosis is mutualistic, where the host benefits from symbiont photosynthesis while providing protection and photosynthetic substrates. Diverse assemblages of symbiotic gorgonian octocorals can be found in hard bottom communities throughout the Caribbean. While current research has focused on the phylo- and population genetics of gorgonian symbiont types and their photo-physiology, relatively less work has focused on biogeochemical benefits conferred to the host and how these benefits vary across host species. Here, we examine this symbiosis among 11 gorgonian species collected in Bocas del Toro, Panama. By coupling light and dark bottle incubations (P/R) with 13C-bicarbonate tracers, we quantified the link between holobiont oxygen metabolism with carbon assimilation and translocation from symbiont to host. Our data show that P/R varied among species, and was correlated with colony morphology and polyp size. Sea fans and sea plumes were net autotrophs (P/R > 1.5) while nine species of sea rods were net heterotrophs with most below compensation (P/R < 1.0). 13C assimilation corroborated the P/R results, and maximum δ13Chost values were strongly correlated with polyp size, indicating higher productivity by colonies with high polyp SA:V. A survey of gorgonian-Symbiodinium associations revealed that productive species maintain specialized, obligate symbioses and are more resistant to coral bleaching, whereas generalist and facultative associations are common among sea rods that have higher bleaching sensitivities. Overall, productivity and polyp size had strong phylogenetic signals with carbon fixation and polyp size showing evidence of trait covariance.published_or_final_versio

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