Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo-Pacific reef-building corals.

Reef-building corals in the genus Porites are one of the most important constituents of Indo-Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, some Porites exhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals, Porites rus and Porites cylindrica, from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genus Cladocopium (within the ITS2 C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to each Porites species living in each reef habitat. Furthermore, these closely related Cladocopium lineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts within P. cylindrica were relatively unaffected by exposure to 32℃ for 14 days, whereas P. rus colonies lost substantial numbers of photochemically compromised symbionts. Heating reduced the ability of the offshore symbiont associated with P. rus to translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshore P. cylindrica. This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef-building Porites.

Transcriptional response of two core photosystem genes in Symbiodinium spp. exposed to thermal stress.

Mutualistic symbioses between scleractinian corals and endosymbiotic dinoflagellates (Symbiodinium spp.) are the foundation of coral reef ecosystems. For many coral-algal symbioses, prolonged episodes of thermal stress damage the symbiont's photosynthetic capability, resulting in its expulsion from the host. Despite the link between photosynthetic competency and symbiont expulsion, little is known about the effect of thermal stress on the expression of photosystem genes in Symbiodinium. This study used real-time PCR to monitor the transcript abundance of two important photosynthetic reaction center genes, psbA (encoding the D1 protein of photosystem II) and psaA (encoding the P(700) protein of photosystem I), in four cultured isolates (representing ITS2-types A13, A20, B1, and F2) and two in hospite Symbiodinium spp. within the coral Pocillopora spp. (ITS2-types C1b-c and D1). Both cultured and in hospite Symbiodinium samples were exposed to elevated temperatures (32°C) over a 7-day period and examined for changes in photochemistry and transcript abundance. Symbiodinium A13 and C1b-c (both thermally sensitive) demonstrated significant declines in both psbA and psaA during the thermal stress treatment, whereas the transcript levels of the other Symbiodinium types remained stable. The downregulation of both core photosystem genes could be the result of several different physiological mechanisms, but may ultimately limit repair rates of photosynthetic proteins, rendering some Symbiodinium spp. especially susceptible to thermal stress.

Genotypic diversity and spatial-temporal distribution of Symbiodinium clones in an abundant reef coral.

Genetic data are rapidly advancing our understanding of various biological systems including the ecology and evolution of coral-algal symbioses. The fine-scale interactions between individual genotypes of host and symbiont remain largely unstudied and constitute a major gap in knowledge. By applying microsatellite markers developed for both host and symbiont, we investigated the intracolony diversity, prevalence and stability of Symbiodinium glynni (type D1) multilocus genotypes in association with dense populations of Pocillopora at two sites in the Gulf of California. The genetic diversity and allelic frequencies in reef populations of S. glynni remained stable over 3 years. Common clone genotypes persisted over this period, and no temporal population subdivision (Φ(PT) = 0.021 and -0.003) was detected. Collections from circular plots showed no statistical correlation between related Pocillopora individuals and their associations with particular S. glynni genotypes, with no spatial structuring or clonal aggregation across a reef for the symbiont. From permanent linear transects, samples were analysed from multiple locations within a colony and some were resampled approximately 1 year later. Many of these multisampled colonies (approximately 53%) were dominated by a single S. glynni genotype and tended to associate with the same symbiont genotype(s) over time, while colony ramets often possessed unrelated symbiont genotypes. In contrast to the species level, associations between genotypes of Pocillopora and S. glynni are apparently more flexible over space and time. The abundance of sexually recombinant genotypes of S. glynni combined with greater flexibility might provide adaptive mechanisms for these symbioses to evolve rapidly to changes in environmental conditions and allow particular symbiont genotypes to spread through a host population.

Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance.

Mutualisms between reef-building corals and endosymbiotic dinoflagellates are particularly sensitive to environmental stress, yet the ecosystems they construct have endured major oscillations in global climate. During the winter of 2008, an extreme cold-water event occurred in the Gulf of California that bleached corals in the genus Pocillopora harbouring a thermally 'sensitive' symbiont, designated Symbiodinium C1b-c, while colonies possessing Symbiodinium D1 were mostly unaffected. Certain bleached colonies recovered quickly while others suffered partial or complete mortality. In most colonies, no appreciable change was observed in the identity of the original symbiont, indicating that these partnerships are stable. During the initial phases of recovery, a third species of symbiont B1(Aiptasia), genetically identical to that harboured by the invasive anemone, Aiptasia sp., grew opportunistically and was visible as light-yellow patches on the branch tips of several colonies. However, this symbiont did not persist and was displaced in all cases by C1b-c several months later. Colonies with D1 were abundant at inshore habitats along the continental eastern Pacific, where seasonal turbidity is high relative to offshore islands. Environmental conditions of the central and southern coasts of Mexico were not sufficient to explain the exclusivity of D1 Pocillopora in these regions. It is possible that mass mortalities associated with major thermal disturbances during the 1997-1998 El Niño Southern Oscillation eliminated C1b-c holobionts from these locations. The differential loss of Pocillopora holobionts in response to thermal stress suggests that natural selection on existing variation can cause rapid and significant shifts in the frequency of particular coral-algal partnerships. However, coral populations may take decades to recover following episodes of severe selection, thereby raising considerable uncertainty about the long-term viability of these communities.

Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in 'stress-tolerant' clade D Symbiodinium.

Reef corals harbouring clade D Symbiodinium spp. (endosymbiotic dinoflagellates) appear more tolerant of environmental stress. As sea surface temperatures rise, symbioses involving Symbiodinium D may increase in prevalence. For this reason, eight polymorphic microsatellite loci were developed for clade D Symbiodinium. From the analysis of 132 samples originating from cnidarian hosts in the Atlantic, Pacific and Indian Oceans, 4 to 35 alleles were found at each haploid locus and diversity indices ranged from 0.35 to 0.97. Population genetic analyses of these symbionts should reveal how environmental perturbations affect genetic diversity, geographical distributions, and possible host-range expansions to new coral species.