Ruth D. Gates

Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching

During the past decade, acute and chronic bleaching of tropical reef corals has occurred with increasing frequency and scale. Bleaching, i.e., the loss of pigment and the decrease in population density of symbiotic dinoflagellates (zooxanthellae), is often correlated with an increase or decrease in sea surface temperature. Because little is known of the cellular events concomitant with thermal bleaching, we have investigated the mechanism of release of zooxanthellae by the tropical sea anemone Aiptasia pulchella and the reef coral Pocillopora damicornis in response to cold and heat stress. Both species released intact host endoderm cells containing zooxanthellae. The majority of the released host cells were viable, but they soon disintegrated in the seawater leaving behind isolated zooxanthellae. The detachment and release of intact host cells suggests that thermal stress causes host cell adhesion dysfunction in these cnidarians. Knowledge of the cellular entity released by the host during bleaching provides insight into both the underlying release mechanism and the way in which natural environmental stresses evoke a bleaching response.

The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing.

Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the worlds oceans.

Conservation genetics and the resilience of reef‐building corals

Coral reefs have suffered long‐term decline due to a range of anthropogenic disturbances and are now also under threat from climate change. For appropriate management of these vulnerable and valuable ecosystems it is important to understand the factors and processes that determine their resilience and that of the organisms inhabiting them, as well as those that have led to existing patterns of coral reef biodiversity. The scleractinian (stony) corals deposit the structural framework that supports and promotes the maintenance of biological diversity and complexity of coral reefs, and as such, are major components of these ecosystems. The success of reef‐building corals is related to their obligate symbiotic association with dinoflagellates of the genus Symbiodinium. These one‐celled algal symbionts (zooxanthellae) live in the endodermal tissues of their coral host, provide most of the hosts energy budget and promote rapid calcification. Furthermore, zooxanthellae are the main primary producers on coral reefs due to the oligotrophic nature of the surrounding waters. In this review paper, we summarize and critically evaluate studies that have employed genetics and/or molecular biology in examining questions relating to the evolution and ecology of reef‐building corals and their algal endosymbionts, and that bear relevance to coral reef conservation. We discuss how these studies can focus future efforts, and examine how these approaches enhance our understanding of the resilience of reef‐building corals.

Functional diversity in coral–dinoflagellate symbiosis

Symbioses are widespread in nature and occur along a continuum from parasitism to mutualism. Coral–dinoflagellate symbioses are defined as mutualistic because both partners receive benefit from the association via the exchange of nutrients. This successful interaction underpins the growth and formation of coral reefs. The symbiotic dinoflagellate genus Symbiodinium is genetically diverse containing eight divergent lineages (clades A–H). Corals predominantly associate with clade C Symbiodinium and to a lesser extent with clades A, B, D, F, and G. Variation in the function and interactive physiology of different coral–dinoflagellate assemblages is virtually unexplored but is an important consideration when developing the contextual framework of factors that contribute to coral reef resilience. In this study, we present evidence that clade A Symbiodinium are functionally less beneficial to corals than the dominant clade C Symbiodinium and may represent parasitic rather than mutualistic symbionts. Our hypothesis is supported by (i) a significant correlation between the presence of Symbiodinium clade A and health-compromised coral; (ii) a phylogeny and genetic diversity within Symbiodinium that suggests a different evolutionary trajectory for clade A compared with the other dominant Symbiodinium lineages; and (iii) a significantly lower amount of carbon fixed and released by clade A in the presence of a coral synthetic host factor as compared with the dominant coral symbiont lineage, clade C. Collectively, these data suggest that along the symbiotic continuum the interaction between clade A Symbiodinium and corals may be closer to parasitism than mutualism.

Building coral reef resilience through assisted evolution

The genetic enhancement of wild animals and plants for characteristics that benefit human populations has been practiced for thousands of years, resulting in impressive improvements in commercially valuable species. Despite these benefits, genetic manipulations are rarely considered for noncommercial purposes, such as conservation and restoration initiatives. Over the last century, humans have driven global climate change through industrialization and the release of increasing amounts of CO2, resulting in shifts in ocean temperature, ocean chemistry, and sea level, as well as increasing frequency of storms, all of which can profoundly impact marine ecosystems. Coral reefs are highly diverse ecosystems that have suffered massive declines in health and abundance as a result of these and other direct anthropogenic disturbances. There is great concern that the high rates, magnitudes, and complexity of environmental change are overwhelming the intrinsic capacity of corals to adapt and survive. Although it is important to address the root causes of changing climate, it is also prudent to explore the potential to augment the capacity of reef organisms to tolerate stress and to facilitate recovery after disturbances. Here, we review the risks and benefits of the improvement of natural and commercial stocks in noncoral reef systems and advocate a series of experiments to determine the feasibility of developing coral stocks with enhanced stress tolerance through the acceleration of naturally occurring processes, an approach known as (human)-assisted evolution, while at the same time initiating a public dialogue on the risks and benefits of this approach.

The future of coral reefs: a microbial perspective

Microbial communities respond and quickly adapt to disturbance and have central roles in ecosystem function. Yet, the many roles of coral-associated microbial communities are not currently accounted for in predicting future responses of reef ecosystems. Here, we propose that a clearer understanding of coral-associated microbial diversity and its interaction with both host and environment will identify important linkages occurring between the microbial communities and macroecological change. Characterizing these links is fundamental to understanding coral reef resilience and will improve our capacity to predict ecological change.

The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts.

Despite being one of the simplest metazoans, corals harbor some of the most highly diverse and abundant microbial communities. Differentiating core, symbiotic bacteria from this diverse host-associated consortium is essential for characterizing the functional contributions of bacteria but has not been possible yet. Here we characterize the coral core microbiome and demonstrate clear phylogenetic and functional divisions between the micro-scale, niche habitats within the coral host. In doing so, we discover seven distinct bacterial phylotypes that are universal to the core microbiome of coral species, separated by thousands of kilometres of oceans. The two most abundant phylotypes are co-localized specifically with the corals’ endosymbiotic algae and symbiont-containing host cells. These bacterial symbioses likely facilitate the success of the dinoflagellate endosymbiosis with corals in diverse environmental regimes.

Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity?

The degree to which coral reef ecosystems will be impacted by global climate change depends on regional and local differences in corals’ susceptibility and resilience to environmental stressors. Here, we present data from a reciprocal transplant experiment using the common reef building coral Porites lobata between a highly fluctuating back reef environment that reaches stressful daily extremes, and a more stable, neighbouring forereef. Protein biomarker analyses assessing physiological contributions to stress resistance showed evidence for both fixed and environmental influence on biomarker response. Fixed influences were strongest for ubiquitin‐conjugated proteins with consistently higher levels found in back reef source colonies both pre and post‐transplant when compared with their forereef conspecifics. Additionally, genetic comparisons of back reef and forereef populations revealed significant population structure of both the nuclear ribosomal and mitochondrial genomes of the coral host (FST = 0.146 P < 0.0001, FST = 0.335 P < 0.0001 for rDNA and mtDNA, respectively), whereas algal endosymbiont populations were genetically indistinguishable between the two sites. We propose that the genotype of the coral host may drive limitations to the physiological responses of these corals when faced with new environmental conditions. This result is important in understanding genotypic and environmental interactions in the coral algal symbiosis and how corals may respond to future environmental changes.

Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics

Most studies on coral reefs have focused on shallow reef (< 30 m) systems due to the technical limitations of conducting scientific diving deeper than 30 m. Compared to their shallow-water counterparts, these mesophotic coral reefs (30-150 m) are understudied, which has slowed our broader understanding of the biodiversity, ecology, and connectivity of shallow and deep coral reef communities. We know that the light environment is an important component of the productivity, physiology, and ecology of corals, and it restricts the distribution of most species of coral to depths of 60 m or less. In the Bahamas, the coral Montastraea cavernosa has a wide depth distribution, and it is one of the most numerous corals at mesophotic depths. Using a range of optical, physiological, and biochemical approaches, the relative dependence on autotrophy vs. heterotrophy was assessed for this coral from 3 to 91 m. These measurements show that the quantum yield of PSII fluorescence increases significantly with depth for M. cavernosa while gross primary productivity decreases with depth. Both morphological and physiological photoacclimatization occurs to a depth of 91 m, and stable isotope data of the host tissues, symbionts, and skeleton reveal a marked decrease in productivity and a sharp transition to heterotrophy between 45 and 61 m. Below these depths, significant changes in the genetic composition of the zooxanthellae community, including genotypes not previously observed, occur and suggest that there is strong selection for zooxanthellae that are suited for survival in the light-limited environment where mesophotic M. cavernosa are occurring.

Seawater temperature and sublethal coral bleaching in Jamaica

Permanent study sites were established at 6 m, 12 m and 18 m on the West Fore Reef at Discovery Bay, Jamaica. Colonies of Montastrea annularis, Porites astreoides, Porites porites and Agaricia spp. were assessed for presence and extent of bleached tissue at two month intervals between October 1986 and September 1987. In 98% of all corals exhibiting a bleaching response, less than 25% of the colony appeared pale. In the remaining 2%, more than 25% of the tissue appeared pale. M. annularis, P. astreoides and Agaricia spp. showed a significant positive correlation between the percent of colonies exhibiting a partial bleaching response and seawater temperature. There was no significant difference in the percentage of colonies bleached between the three depths. M. annularis and Agaricia spp. exhibited a significantly higher percentage of colonies bleached than P. astreoides and P. porites. For M. annularis 15% of coral colonies studied showed 1–2 cm2 randomly seattered patches of pale tissue which remained constant throughout the study. The partial bleaching patterns observed in this study were never lethal and are considered, in part, to be a response to seasonal variations in seawater temperature.