Highlights • Nitrogen cycling in reef-building corals is a function of all holobiont members. • Control of nitrogen cycling may stabilize holobiont functioning under oligotrophic and eutrophic ...conditions. • Anthropogenic change may sway the control of nitrogen cycling, promoting coral decline. • Elevated nitrogen fixation rates may foster coral bleaching and disease.
Animals and plants are metaorganisms and associate with microbes that affect their physiology, stress tolerance, and fitness. Here the hypothesis that alteration of the microbiome may constitute a ...fast‐response mechanism to environmental change is examined. This is supported by recent reciprocal transplant experiments with reef corals, which have shown that their microbiome adapts to thermally variable habitats and changes over time when transplanted into different environments. Further, inoculation of corals with beneficial bacteria increases their stress tolerance. But corals differ in their ability to flexibly associate with different bacteria. How scales of microbiome flexibility may reflect different metaorganism adaptation mechanisms is discussed and future directions for research are pinpointed. It is posited that microbiome flexibility is a broad phenomenon that contributes to the ability of organisms to respond to environmental change. Importantly, adapting with microbial help may provide an alternate route to organismal adaptation that facilitates rapid responses.
In this work, microbiome flexibility, i.e. the potential for dynamic restructuring of the host microbiome, as a fast‐response mechanism to environmental change is examined. How scales of microbiome flexibility may reflect different metaorganism adaptation mechanisms and future research directions are discussed. Adapting with microbial help may provide an alternate route to organismal adaptation that facilitates rapid responses.
The advent of molecular data has transformed the science of organizing and studying life on Earth. Genetics-based evidence provides fundamental insights into the diversity, ecology, and origins of ...many biological systems, including the mutualisms between metazoan hosts and their micro-algal partners. A well-known example is the dinoflagellate endosymbionts (“zooxanthellae”) that power the growth of stony corals and coral reef ecosystems. Once assumed to encompass a single panmictic species, genetic evidence has revealed a divergent and rich diversity within the zooxanthella genus Symbiodinium. Despite decades of reporting on the significance of this diversity, the formal systematics of these eukaryotic microbes have not kept pace, and a major revision is long overdue. With the consideration of molecular, morphological, physiological, and ecological data, we propose that evolutionarily divergent Symbiodinium “clades” are equivalent to genera in the family Symbiodiniaceae, and we provide formal descriptions for seven of them. Additionally, we recalibrate the molecular clock for the group and amend the date for the earliest diversification of this family to the middle of the Mesozoic Era (∼160 mya). This timing corresponds with the adaptive radiation of analogs to modern shallow-water stony corals during the Jurassic Period and connects the rise of these symbiotic dinoflagellates with the emergence and evolutionary success of reef-building corals. This improved framework acknowledges the Symbiodiniaceae’s long evolutionary history while filling a pronounced taxonomic gap. Its adoption will facilitate scientific dialog and future research on the physiology, ecology, and evolution of these important micro-algae.
•The micro-algal genus Symbiodinium is split into multiple genera•Seven of these genera are formally described based on genetics and ecology•Dinoflagellates in the family Symbiodiniaceae originated in the Jurassic Period•Symbiodiniaceae diversification coincided with the radiation of reef-building corals
Symbiodinium are micro-algal symbionts of reef-building corals. LaJeunesse et al. report new estimates from molecular dating, indicating that corals and Symbiodinium originated and diversified together ∼140–200 mya. Divergent Symbiodinium “clades” are now partitioned into multiple genera, better reflecting their long evolutionary history.
Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse ...microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.
Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been ...extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral
to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.
Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium ...are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2-3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the "overlooked" coral skeleton.
Dinoflagellates are unicellular algae that are ubiquitously abundant in aquatic environments. Species of the genus Symbiodinium form symbiotic relationships with reef-building corals and other marine ...invertebrates. Despite their ecologic importance, little is known about the genetics of dinoflagellates in general and Symbiodinium in particular. Here, we used 454 sequencing to generate transcriptome data from two Symbiodinium species from different clades (clade A and clade B). With more than 56,000 assembled sequences per species, these data represent the largest transcriptomic resource for dinoflagellates to date. Our results corroborate previous observations that dinoflagellates possess the complete nucleosome machinery. We found a complete set of core histones as well as several H3 variants and H2A.Z in one species. Furthermore, transcriptome analysis points toward a low number of transcription factors in Symbiodinium spp. that also differ in the distribution of DNA-binding domains relative to other eukaryotes. In particular the cold shock domain was predominant among transcription factors. Additionally, we found a high number of antioxidative genes in comparison to non-symbiotic but evolutionary related organisms. These findings might be of relevance in the context of the role that Symbiodinium spp. play as coral symbionts.Our data represent the most comprehensive dinoflagellate EST data set to date. This study provides a comprehensive resource to further analyze the genetic makeup, metabolic capacities, and gene repertoire of Symbiodinium and dinoflagellates. Overall, our findings indicate that Symbiodinium possesses some unique characteristics, in particular the transcriptional regulation in Symbiodinium may differ from the currently known mechanisms of eukaryotic gene regulation.
Coral reefs rely upon the highly optimized coral–Symbiodiniaceae symbiosis, making them sensitive to environmental change and susceptible to anthropogenic stress. Coral bleaching is predominantly ...attributed to photo-oxidative stress, yet nutrient availability and metabolism underpin the stability of symbioses. Recent studies link symbiont proliferation under nutrient enrichment to bleaching; however, the interactions between nutrients and symbiotic stability are nuanced. Here, we demonstrate how bleaching is regulated by the forms and ratios of available nutrients and their impacts on autotrophic carbon metabolism, rather than algal symbiont growth. By extension, historical nutrient conditions mediate host–symbiont compatibility and bleaching tolerance over proximate and evolutionary timescales. Renewed investigations into the coral nutrient metabolism will be required to truly elucidate the cellular mechanisms leading to coral bleaching.
Mass coral bleaching is occurring at an unprecedented rate due to anthropogenic ocean warming, and it represents the greatest threat to coral reef ecosystems globally.Coral bleaching is predominantly attributed to photo-oxidative stress under elevated temperature and light, but recent experiments have unveiled nutritional mechanisms that can regulate bleaching.Bleaching may result when the coral–Symbiodiniaceae symbiosis shifts from a mutualistic to a parasitic relationship under thermal stress.Nutrient availability, specifically the forms and ratios of nutrients such as nitrogen and phosphorus, mediates algal symbiont parasitism.Stable metabolic compatibility between the coral host and algal symbiont can ameliorate bleaching and increase resilience to environmental stress.
Algal symbionts (zooxanthellae, genus Symbiodinium) of scleractinian corals respond strongly to temperature, nutrient and light changes. These factors vary greatly along the north-south gradient in ...the Red Sea and include conditions, which are outside of those typically considered optimal for coral growth. Nevertheless, coral communities thrive throughout the Red Sea, suggesting that zooxanthellae have successfully acclimatized or adapted to the harsh conditions they experience particularly in the south (high temperatures and high nutrient supply). As such, the Red Sea is a region, which may help to better understand how zooxanthellae and their coral hosts successfully acclimatize or adapt to environmental change (e.g. increased temperatures and localized eutrophication). To gain further insight into the physiology of coral symbionts in the Red Sea, we examined the abundance of dominant Symbiodinium types associated with the coral Pocillopora verrucosa, and measured Symbiodinium physiological characteristics (i.e. photosynthetic processes, cell density, pigmentation, and protein composition) along the latitudinal gradient of the Red Sea in summer and winter. Despite the strong environmental gradients from north to south, our results demonstrate that Symbiodinium microadriaticum (type A1) was the predominant species in P. verrucosa along the latitudinal gradient. Furthermore, measured physiological characteristics were found to vary more with prevailing seasonal environmental conditions than with region-specific differences, although the measured environmental parameters displayed much higher spatial than temporal variability. We conclude that our findings might present the result of long-term acclimatization or adaptation of S. microadriaticum to regionally specific conditions within the Red Sea. Of additional note, high nutrients in the South correlated with high zooxanthellae density indicating a compensation for a temperature-driven loss of photosynthetic performance, which may prove promising for the resilience of these corals under increase of temperature increase and eutrophication.
Deserts, such as those found in Saudi Arabia, are one of the most hostile places for plant growth. However, desert plants are able to impact their surrounding microbial community and select ...beneficial microbes that promote their growth under these extreme conditions. In this study, we examined the soil, rhizosphere and endosphere bacterial communities of four native desert plants Tribulus terrestris, Zygophyllum simplex, Panicum turgidum and Euphorbia granulata from the Southwest (Jizan region), two of which were also found in the Midwest (Al Wahbah area) of Saudi Arabia. While the rhizosphere bacterial community mostly resembled that of the highly different surrounding soils, the endosphere composition was strongly correlated with its host plant phylogeny. In order to assess whether any of the native bacterial endophytes might have a role in plant growth under extreme conditions, we analyzed the properties of 116 cultured bacterial isolates that represent members of the phyla Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes. Our analysis shows that different strains have highly different biochemical properties with respect to nutrient acquisition, hormone production and growth under stress conditions. More importantly, eleven of the isolated strains could confer salinity stress tolerance to the experimental model plant Arabidopsis thaliana suggesting some of these plant-associated bacteria might be useful for improving crop desert agriculture.
PDF
