Dataset Information

Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.

ABSTRACT: 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.

SUBMITTER: Kirk NL

PROVIDER: S-EPMC3833926 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.

Kirk Nathan L NL Ritson-Williams Raphael R Coffroth Mary Alice MA Miller Margaret W MW Fogarty Nicole D ND Santos Scott R SR

PloS one 20131119 11

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, ...[more]

PMID: 24260438

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Project description:Global climate change not only leads to elevated seawater temperatures but also to episodic anomalously high or low temperatures lasting for several hours to days. Scleractinian corals are detrimentally affected by thermal fluctuations, which often lead to an uncoupling of their mutualism with Symbiodinium spp. (coral bleaching) and potentially coral death. Consequently, on many Caribbean reefs scleractinian coral cover has plummeted. Conversely, gorgonian corals persist, with their abundance even increasing. How gorgonians react to thermal anomalies has been investigated utilizing limited parameters of either the gorgonian, Symbiodinium or the combined symbiosis (holobiont). We employed a holistic approach to examine the effect of an experimental five-day elevated temperature episode on parameters of the host, symbiont, and the holobiont in Eunicea tourneforti, E. flexuosa and Pseudoplexaura porosa. These gorgonian corals reacted and coped with 32°C seawater temperatures. Neither Symbiodinium genotypes nor densities differed between the ambient 29.5°C and 32°C. Chlorophyll a and c2 per Symbiodinium cell, however, were lower at 32°C leading to a reduction in chlorophyll content in the branches and an associated reduction in estimated absorbance and increase in the chlorophyll a specific absorption coefficient. The adjustments in the photochemical parameters led to changes in photochemical efficiencies, although these too showed that the gorgonians were coping. For example, the maximum excitation pressure, Qm, was significantly lower at 32°C than at 29.5°C. In addition, although per dry weight the amount of protein and lipids were lower at 32°C, the overall energy content in the tissues did not differ between the temperatures. Antioxidant activity either remained the same or increased following exposure to 32°C further reiterating a response that dealt with the stressor. Taken together, the capability of Caribbean gorgonian corals to modify symbiont, host and consequently holobiont parameters may partially explain their persistence on reefs faced with climate change.

Project description:BackgroundApicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. A novel group of apicomplexans, recently named corallicolids, have been detected in corals inhabiting tropical shallow reefs. These apicomplexans may represent a transitional lifestyle between free-living phototrophs and obligate parasites. To shed light on the evolutionary history of apicomplexans and to investigate their ecology in association with corals, we screened scleractinians, antipatharians, alcyonaceans, and zoantharians from shallow, mesophotic, and deep-sea communities. We detected corallicolid plastids using 16S metabarcoding, sequenced the nuclear 18S rRNA gene of corallicolids from selected samples, assembled and annotated the plastid and mitochondrial genomes from a corallicolid that associates with a deep-sea coral, and screened the metagenomes of four coral species for corallicolids.ResultsWe detected 23 corallicolid plastotypes that were associated with 14 coral species from three orders and depths down to 1400 m. Individual plastotypes were restricted to coral hosts within a single depth zone and within a single taxonomic order of corals. Some clusters of closely related corallicolids were revealed that associated with closely related coral species. However, the presence of divergent corallicolid lineages that associated with similar coral species and depths suggests that corallicolid/coral relations are flexible over evolutionary timescales and that a large diversity of apicomplexans may remain undiscovered. The corallicolid plastid genome from a deep-sea coral contained four genes involved in chlorophyll biosynthesis: the three genes of the LIPOR complex and acsF.ConclusionsThe presence of corallicolid apicomplexans in corals below the photic zone demonstrates that they are not restricted to shallow-water reefs and are more general anthozoan symbionts. The presence of LIPOR genes in the deep-sea corallicolid precludes a role involving photosynthesis and suggests they may be involved in a different function. Thus, these genes may represent another set of genetic tools whose function was adapted from photosynthesis as the ancestors of apicomplexans evolved towards parasitic lifestyles. Video abstract.

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Project description:BackgroundThe microbiomes of foundation (habitat-forming) species such as corals and sponges underpin the biodiversity, productivity, and stability of ecosystems. Consumers shape communities of foundation species through trophic interactions, but the role of consumers in dispersing the microbiomes of such species is rarely examined. For example, stony corals rely on a nutritional symbiosis with single-celled endosymbiotic dinoflagellates (family Symbiodiniaceae) to construct reefs. Most corals acquire Symbiodiniaceae from the environment, but the processes that make Symbiodiniaceae available for uptake are not resolved. Here, we provide the first comprehensive, reef-scale demonstration that predation by diverse coral-eating (corallivorous) fish species promotes the dispersal of Symbiodiniaceae, based on symbiont cell densities and community compositions from the feces of four obligate corallivores, three facultative corallivores, two grazer/detritivores as well as samples of reef sediment and water.ResultsObligate corallivore feces are environmental hotspots of Symbiodiniaceae cells: live symbiont cell concentrations in such feces are 5-7 orders of magnitude higher than sediment and water environmental reservoirs. Symbiodiniaceae community compositions in the feces of obligate corallivores are similar to those in two locally abundant coral genera (Pocillopora and Porites), but differ from Symbiodiniaceae communities in the feces of facultative corallivores and grazer/detritivores as well as sediment and water. Combining our data on live Symbiodiniaceae cell densities in feces with in situ observations of fish, we estimate that some obligate corallivorous fish species release over 100 million Symbiodiniaceae cells per 100 m2 of reef per day. Released corallivore feces came in direct contact with coral colonies in the fore reef zone following 91% of observed egestion events, providing a potential mechanism for the transfer of live Symbiodiniaceae cells among coral colonies.ConclusionsTaken together, our findings show that fish predation on corals may support the maintenance of coral cover on reefs in an unexpected way: through the dispersal of beneficial coral symbionts in corallivore feces. Few studies examine the processes that make symbionts available to foundation species, or how environmental reservoirs of such symbionts are replenished. This work sets the stage for parallel studies of consumer-mediated microbiome dispersal and assembly in other sessile, habitat-forming species.

Dataset Information

Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.

Publications

Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.

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