Climate change promotes parasitism in a coral symbiosis.

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26 °C) and sub-bleaching (31 °C) temperatures under elevated nitrate. Warming to 31 °C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change

Improved Resolution of Reef-Coral Endosymbiont (Symbiodinium) Species Diversity, Ecology, and Evolution through psbA Non-Coding Region Genotyping

Ribosomal DNA sequence data abounds from numerous studies on the dinoflagellate endosymbionts of corals, and yet the multi-copy nature and intragenomic variability of rRNA genes and spacers confound interpretations of symbiont diversity and ecology. Making consistent sense of extensive sequence variation in a meaningful ecological and evolutionary context would benefit from the application of additional genetic markers. Sequences of the non-coding region of the plastid psbA minicircle (psbAncr) were used to independently examine symbiont genotypic and species diversity found within and between colonies of Hawaiian reef corals in the genus Montipora. A single psbAncr haplotype was recovered in most samples through direct sequencing (∼80–90%) and members of the same internal transcribed spacer region 2 (ITS2) type were phylogenetically differentiated from other ITS2 types by substantial psbAncr sequence divergence. The repeated sequencing of bacterially-cloned fragments of psbAncr from samples and clonal cultures often recovered a single numerically common haplotype accompanied by rare, highly-similar, sequence variants. When sequence artifacts of cloning and intragenomic variation are factored out, these data indicate that most colonies harbored one dominant Symbiodinium genotype. The cloning and sequencing of ITS2 DNA amplified from these same samples recovered numerically abundant variants (that are diagnostic of distinct Symbiodinium lineages), but also generated a large amount of sequences comprising PCR/cloning artifacts combined with ancestral and/or rare variants that, if incorporated into phylogenetic reconstructions, confound how small sequence differences are interpreted. Finally, psbAncr sequence data from a broad sampling of Symbiodinium diversity obtained from various corals throughout the Indo-Pacific were concordant with ITS lineage membership (defined by denaturing gradient gel electrophoresis screening), yet exhibited substantially greater sequence divergence and revealed strong phylogeographic structure corresponding to major biogeographic provinces. The detailed genetic resolution provided by psbAncr data brings further clarity to the ecology, evolution, and systematics of symbiotic dinoflagellates

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

Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation

© 2015 New Phytologist Trust. Dinoflagellates of the genus Symbiodinium express broad diversity in both genetic identity (phylogeny) and photosynthetic function to presumably optimize ecological success across extreme light environments; however, whether differences in the primary photobiological characteristics that govern photosynthetic optimization are ultimately a function of phylogeny is entirely unresolved. We applied a novel fast repetition rate fluorometry approach to screen genetically distinct Symbiodinium types (n=18) spanning five clades (A-D, F) for potential phylogenetic trends in factors modulating light absorption (effective cross-section, reaction center content) and utilization (photochemical vs dynamic nonphotochemical quenching; [1 - C] vs [1 - Q]) by photosystem II (PSII). The variability of PSII light absorption was independent of phylogenetic designation, but closely correlated with cell size across types, whereas PSII light utilization intriguingly followed one of three characteristic patterns: (1) similar reliance on [1 - C] and [1 - Q] or (2) preferential reliance on [1 - C] (mostly A, B types) vs (3) preferential reliance on [1 - Q] (mostly C, D, F types), and thus generally consistent with cladal designation. Our functional trait-based approach shows, for the first time, how Symbiodinium photosynthetic function is governed by the interplay between phylogenetically dependent and independent traits, and is potentially a means to reconcile complex biogeographic patterns of Symbiodinium phylogenetic diversity in nature

Erratum: Correction to: Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities (Microbiome (2020) 8 1 (8))

Following publication of the original article [1], the authors reported an error on the legend of of P.damicornis in Fig. 1

Organic carbon fluxes mediated by corals at elevated pCO2 and temperature

Increasing ocean acidification (OA) and seawater temperatures pose significant threats to coral reefs globally. While the combined impacts of OA and seawater temperature on coral biology and calcification in corals have received significant study, research to date has largely neglected the individual and combined effects of OA and seawater temperature on coral-mediated organic carbon (OC) fluxes. This is of particular concern as dissolved and particulate OC (DOC and POC, respectively) represent large pools of fixed OC on coral reefs. In the present study, coral-mediated POC and DOC, and the sum of these coral-mediated flux rates (total OC, TOC = DOC + POC) as well as the relative contributions of each to coral metabolic demand were determined for 2 species of coral, Acropora millepora and Turbinaria reniformis, at 2 levels of pCO2 (382 and 741 µatm) and seawater temperatures (26.5 and 31.0°C). Independent of temperature, DOC fluxes decreased significantly with increases in pCO2 in both species, resulting in more DOC being retained by the corals and only representing between 19 and 6% of TOC fluxes for A. millepora and T. reniformis. At the same time, POC and TOC fluxes were unaffected by elevated temperature and/or pCO2. These findings add to a growing body of evidence that certain species of coral may be less at risk to the impacts of OA and temperature than previously thought

Isolation, characterisation and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C)

The health and productivity of coral reefs is underpinned by the symbiosis between corals and dinoflagellates\ud (Symbiodinium spp.). To enable population genetic analyses of Symbiodinium spp, required for coral reef conservation, seven microsatellite loci were isolated from Symbiodinium clade C from the Great Barrier Reef, Australia. These microsatellite primer pairs consistently amplified between 1 and 8 alleles per coral host colony, with mean number of alleles ranging from 1.9 to 4.0 and generally high genetic diversities (Shannon’s Index = 0.71–2.76). The novel microsatellite loci amplified between 1 and 10 alleles in four other C strains, but did not amplify a D strain.\ud Three of six previously published clade C microsatellite loci amplified 1–6 alleles in two or more of five C strains tested. The primers and cross amplifications presented here therefore provide a useful tool for elucidating the population genetic structure of clade C Symbiodinium populations

Decadal environmental ‘memory’ in a reef coral?

West sides of the coral Coelastrea aspera, which had achieved thermo-tolerance after previous experience of high solar irradiance in the field, were rotated through 180o on a reef flat in Phuket, Thailand (7o50´N, 98o25.5´E), in 2000 in a manipulation experiment and secured in this position. In 2010, elevated sea temperatures caused extreme bleaching in these corals, with former west sides of colonies (now facing east) retaining four times higher symbiont densities than the east sides of control colonies, which had not been rotated and which had been subject to a lower irradiance environment than west sides throughout their lifetime. The reduced bleaching susceptibility of the former west sides in 2010, compared to handling controls, suggests that the rotated corals had retained a ‘memory’ of their previous high irradiance history despite living under lower irradiance for 10 years. Such long-term retention of an environmental ‘memory’ raises important questions about the acclimatisation potential of reef corals in a changing climate and the mechanisms by which it is achieved