The symbiosis between reef-building corals and their algal endosymbionts (zooxanthellae of the genus Symbiodinium) is highly sensitive to temperature stress, which makes coral reefs vulnerable to climate change. Thermal tolerance in corals is known to be substantially linked to the type of zooxanthellae they harbour and, when multiple types are present, the relative abundance of types can be experimentally manipulated to increase the thermal limits of individual corals. Although the potential exists for this to translate into substantial thermal acclimatization of coral communities, to date there is no evidence to show that this takes place under natural conditions. In this study, we show field evidence of a dramatic change in the symbiont community of Acropora millepora, a common and widespread Indo-Pacific hard coral species, after a natural bleaching event in early 2006 in the Keppel Islands (Great Barrier Reef ). Before bleaching, 93.5% (nZ460) of the randomly sampled and tagged colonies predominantly harboured the thermally sensitive Symbiodinium type C2, while the remainder harboured a tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving tagged colonies that were initially C2 predominant changed to D or C1 predominance. Colonies that were originally C2 predominant suffered high mortality (37%) compared with D-predominant colonies (8%). We estimate that just over 18% of the original A. millepora population survived unchanged leaving 29% of the population C2 and 71% D or C1 predominant six months after the bleaching event. This change in the symbiont community structure, while it persists, is likely to have substantially increased the thermal tolerance of this coral population. Understanding the processes that underpin the temporal changes in symbiont communities is key to assessing the acclimatization potential of reef corals.

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Reef corals form associations with an array of genetically and physiologically distinct endosymbionts from the genus Symbiodinium. Some corals harbor different clades of symbionts simultaneously, and over time the relative abundances of these clades may change through a process called symbiont shuffling. It is hypothesized that this process provides a mechanism for corals to respond to environmental threats such as global warming. However, only a minority of coral species have been found to harbor more than one symbiont clade simultaneously and the current view is that the potential for symbiont shuffling is limited. Using a newly developed real-time PCR assay, this paper demonstrates that previous studies have underestimated the presence of background symbionts because of the low sensitivity of the techniques used. The assay used here targets the multi-copy rDNA ITS1 region and is able to detect Symbiodinium clades C and D with >100-fold higher sensitivity compared to conventional techniques. Technical considerations relating to intragenomic variation, estimating copy number and non-symbiotic contamination are discussed. Eighty-two colonies from four common scleractinian species (Acropora millepora, Acropora tenuis, Stylophora pistillata and Turbinaria reniformis) and 11 locations on the Great Barrier Reef were tested for background Symbiodinium clades. Although these colonies had been previously identified as harboring only a single clade based on SSCP analyses, background clades were detected in 78% of the samples, indicating that the potential for symbiont shuffling may be much larger than currently thought.

The potential of corals to associate with more temperature-tolerant strains of algae (zooxanthellae, Symbiodinium) can have important implications for the future of coral reefs in an era of global climate change. In this study, the genetic identity and diversity of zooxanthellae was investigated at three reefs with contrasting histories of bleaching mortality, water temperature and shading, in the Republic of Palau (Micronesia). Single-stranded conformation polymorphism and sequence analysis of the ribosomal DNA internal transcribed spacer (ITS)1 region was used for genotyping. A chronically warm but partly shaded coral reef in a marine lake that is hydrographically well connected to the surrounding waters harboured only two single-stranded conformation polymorphism profiles (i.e. zooxanthella communities). It consisted only of Symbiodinium D in all 13 nonporitid species and two Porites species investigated, with the remaining five Porites harbouring C*. Despite the high temperature in this lake (> 0.5 degrees above ambient), this reef did not suffer coral mortality during the (1998) bleaching event, however, no bleaching-sensitive coral families and genera occur in the coral community. This setting contrasts strongly with two other reefs with generally lower temperatures, in which 10 and 12 zooxanthella communities with moderate to low proportions of clade D zooxanthellae were found. The data indicate that whole coral assemblages, when growing in elevated seawater temperatures and at reduced irradiance, can be composed of colonies associated with the more thermo-tolerant clade D zooxanthellae. Future increases in seawater temperature might, therefore, result in an increasing prevalence of Symbiodinium phylotype D in scleractinian corals, possibly associated with a loss of diversity in both zooxanthellae and corals.

BackgroundReef-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.Methodology/Principal FindingsOffspring 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.Conclusions/SignificanceThese 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.

The presence, genetic identity and diversity of algal endosymbionts (Symbiodinium) in 114 species from 69 genera (20 families) of octocorals from the Great Barrier Reef (GBR), the far eastern Pacific (EP) and the Caribbean was examined, and patterns of the octocoral-algal symbiosis were compared with patterns in the host phylogeny. Genetic analyses of the zooxanthellae were based on ribosomal DNA internal transcribed spacer 1 (ITS1) region. In the GBR samples, Symbiodinium clades A and G were encountered with A and G being rare. Clade B zooxanthellae have been previously reported from a GBR octocoral, but are also rare in octocorals from this region. Symbiodinium G has so far only been found in Foraminifera, but is rare in these organisms. In the Caribbean samples, only Symbiodinium clades B and C are present. Hence, Symbiodinium diversity at the level of phylogenetic clades is lower in octocorals from the Caribbean compared to those from the GBR. However, an unprecedented level of ITS1 diversity was observed within individual colonies of some Caribbean gorgonians, implying either that these simultaneously harbour multiple strains of clade B zooxanthellae, or that ITS1 heterogeneity exists within the genomes of some zooxanthellae. Intracladal diversity based on ITS should therefore be interpreted with caution, especially in cases where no independent evidence exists to support distinctiveness, such as ecological distribution or physiological characteristics. All samples from EP are azooxanthellate. Three unrelated GBR taxa that are described in the literature as azooxanthellate (Junceella fragilis, Euplexaura nuttingi and Stereonephthya sp. 1) contain clade G zooxanthellae, and their symbiotic association with zooxanthellae was confirmed by histology. These corals are pale in colour, whereas related azooxanthellate species are brightly coloured. The evolutionary loss or gain of zooxanthellae may have altered the light sensitivity of the host tissues, requiring the animals to adopt or reduce pigmentation. Finally, we superimposed patterns of the octocoral-algal symbiosis onto a molecular phylogeny of the host. The data show that many losses/gains of endosymbiosis have occurred during the evolution of octocorals. The ancestral state (azooxanthellate or zooxanthellate) in octocorals remains unclear, but the data suggest that on an evolutionary timescale octocorals can switch more easily between mixotrophy and heterotrophy compared to scleractinian corals, which coincides with a low reliance on photosynthetic carbon gain in the former group of organisms.

BackgroundCoral diseases are emerging as a serious threat to coral reefs worldwide. Of nine coral infectious diseases, whose pathogens have been characterized, six are caused by agents from the family Vibrionacae, raising questions as to their origin and role in coral disease aetiology.Methodology/Principal FindingsHere we report on a Vibrio zinc-metalloprotease causing rapid photoinactivation of susceptible Symbiodinium endosymbionts followed by lesions in coral tissue. Symbiodinium photosystem II inactivation was diagnosed by an imaging pulse amplitude modulation fluorometer in two bioassays, performed by exposing Symbiodinium cells and coral juveniles to non-inhibited and EDTA-inhibited supernatants derived from coral white syndrome pathogens.Conclusion/SignificanceThese findings demonstrate a common virulence factor from four phylogenetically related coral pathogens, suggesting that zinc-metalloproteases may play an important role in Vibrio pathogenicity in scleractinian corals.

Understanding the flexibility of the endosymbioses between scleractinian corals and single-cell algae of the genus Symbiodinium will provide valuable insights into the future of coral reefs. Here, a real-time polymerase chain reaction (PCR) assay is presented to accurately determine the cell densities of Symbiodinium clades C and D in the scleractinian coral Acropora millepora, which can be extended to other coral-symbiont associations in the future. The assay targets single- to low-copy genes of the actin family of both the coral host and algal symbiont. Symbiont densities are expressed as the ratio of Symbiodinium cells to each host cell (S/H ratio, error within 30%), but can also be normalized to coral surface area. Greater accuracy in estimating ratios of associations involving multiple clades is achieved compared with previous real-time PCR assays based on high-copy ribosomal DNA loci (error within an order of magnitude). Healthy adult A. millepora containing ~1.4 × 10(6) zooxanthellae per cm(2) (as determined by haemocytometer counts) had S/H ratios of c. 0.15, i.e. ~15 symbiont cells per 100 host cells. In severely bleached colonies, this ratio decreased to less than 0.005. Because of its capacity to accurately determine both densities and ratios of multiple symbionts within one sample, the assay will open the door for novel research into the mechanisms of symbiont shuffling and switching.