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Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Coral photosynthetic endosymbionts (Symbiodinium) are phylogenetically very diverse, yet the extent of inter- and intraspecific functional variation within clades remains largely underexplored. Understanding this variability will be critical for future research on climate change mediated responses. A properly functioning thylakoid membrane is essential for optimal photosynthetic performance both in free living and in hospite conditions. Here, we analyse the thylakoid membrane melting points of 13 Symbiodinium strains from species in Clades B and A, grown at both control (26 °C) and high temperature (31 °C). We observed a broad range of responses to thermal stress regardless of taxonomic rank. Our results support and augment a growing body of the literature demonstrating that functional differences among Symbiodinium spp. are as distinct at lower taxonomic levels (i.e. interspecific) as they are among major clades. These findings highlight the importance of assessing the variability of plastid traits across the Symbiodinium tree.

Polycultures, or multicrops, are groupings of plants that grow more prolifically when planted together as compared to when planted alone as monocultures. One of the best known and widely utilized polycultures is the milpa cropping system - the cultivation of maize, beans, and squash together as “the three sisters.” Milpa has been utilized by the indigenous population of Central America for millennia due to its consistent abundant harvests; today it remains a cornerstone of the region’s tradition, diet, and economic growth. Likely contributing to this legacy is the known association of polycultures and heightened resistance to disease, yet the mechanism underlying this relationship in milpa has largely been unexplored. To assess the health of farm soil exposed to milpa monocrops, bicrops, and multicrops, we measured the growth of two bacterial strains: a Burkholderia strain symbiotic of Anasa tristis (the squash bug, an agricultural pest) and a plant pathogenic Serratia strain that is the primary causal agent of cucurbit yellow vine disease (CYVD). We found that after one week in both the polyculture (corn, bean, and squash) soil and the corn monoculture soil, the growth of Burkholderia was significantly inhibited. However, in both corn & bean and bean & squash biculture soils, the growth of the strain was significantly enhanced. The growth of the Serratia strain did not yield any significant increase or decrease after one week in any milpa soil. We conclude that the cultivation of milpa in its polyculture configuration demonstrates antibiotic activity towards the Burkholderia strain SQ4A. Our investigation supports findings that certain multicrop systems are less susceptible to disease than monocultures possibly due to their greater microbial biomass; thus we can infer a higher amount of root exudates present in the soil, of which a substantial amount may be anti-microbials.

Light and temperature are major drivers in the ecology and biogeography of symbiotic dinoflagellates living in corals and other cnidarians. We examined variations in physiology among 11 strains comprising five species of clade A Symbiodinium . We grew cultures at 26°C (control) and 32°C (high temperature) over a duration of 18 days while measuring growth and photochemical efficiency ( F v / F m ). Responses to thermal stress ranged from susceptible to tolerant across species and strains. Most strains exhibited a decrease in cell densities and F v / F m when grown at 32°C. Tolerance to high temperature ( T 32 ) was calculated for all strains, ranging from 0 (unable to survive at high temperature) to 1 (able survive at high temperature). There was substantial variation in thermotolerance across species and among strains. One strain had a T 32 close to 1, indicating that growth was not reduced at 32°C for only this one strain. To evaluate the combined effect of temperature and light on physiological stress, we selected three strains with different levels of thermotolerance (tolerant, intermediate and susceptible) and grew them under five different light intensities (65, 80, 100, 240 and 443 µmol quanta m −2 s −1 ) at 26 and 32°C. High irradiance exacerbated the effect of high temperature, particularly in strains from thermally sensitive species. This work further supports the recognition that broad physiological differences exist not only among species within Symbiodinium clades, but also among strains within species demonstrating that thermotolerance varies widely between species and among strains within species.

Corals rely on a symbiosis with dinoflagellate algae (Symbiodinium spp.) to thrive in nutrient poor tropical oceans. However, the coral-algal symbiosis can break down during bleaching events, potentially leading to coral death. While genome-wide expression studies have shown the genes associated with the breakdown of this partnership, the full conglomerate of genes responsible for the establishment and maintenance of a healthy symbiosis remains unknown. Results from previous studies suggested little transcriptomic change associated with the establishment of symbiosis. We examined the transcriptomic response of the coral Orbicella faveolata in the presence (symbiotic) and absence (aposymbiotic) of Symbiodinium minutum, one of its associated symbionts. 9 days post-metamorphic aposymbiotic coral polyps of O. faveolata were compared to symbiotic coral polyps and the subsequent differential gene expression between control and treatment was quantified using cDNA microarray technology. Coral polyps exhibited differential expression of genes associated with nutrient metabolism and development, providing insight into control of pathways as a result of symbiosis driving early polyp growth. Furthermore, genes associated with lysosomal fusion were also upregulated, suggesting host regulation of symbiont densities soon after infection.

Coral reefs are threatened by increasing surface seawater temperatures resulting from climate change. Reef-building corals symbiotic with dinoflagellates in the genus Symbiodinium experience dramatic reductions in algal densities when exposed to temperatures above the long-term local summer average, leading to a phenomenon called coral bleaching. Although the temperature-dependent loss in photosynthetic function of the algal symbionts has been widely recognized as one of the early events leading to coral bleaching, there is considerable debate regarding the actual damage site. We have tested the relative thermal stability and composition of membranes in Symbiodinium exposed to high temperature. Our results show that melting curves of photosynthetic membranes from different symbiotic dinoflagellates substantiate a species-specific sensitivity to high temperature, while variations in fatty acid composition under high temperature rather suggest a complex process in which various modifications in lipid composition may be involved. Our results do not support the role of unsaturation of fatty acids of the thylakoid membrane as being mechanistically involved in bleaching nor as being a dependable tool for the diagnosis of thermal susceptibility of symbiotic reef corals.

To date, the association and synchronization between two organismal circadian clocks ticking in parallel as part of a meta-organism (termed a symbiotic association), have rarely been investigated. Reef-building corals exhibit complex rhythmic responses to diurnal, lunar, and annual changes. Understanding circadian, circatidal, and annual regulation in reef-building corals is complicated by the presence of photosynthetic endosymbionts, which have a profound physiochemical influence on the intracellular environment. How corals tune their animal-based clock machinery to respond to external cues while simultaneously responding to internal physiological changes imposed by the symbiont, is not clear. There is insufficient molecular or physiological evidence of the existence of a circadian pacemaker that controls the metabolism, photosynthesis, synchronized mass spawning, and calcification processes in symbiotic corals. In this review, we present current knowledge regarding the animal pacemaker and the symbiotic-algal pacemaker. We examine the evidence from behavioral, physiological, molecular, and evolutionary perspectives. We explain why symbiotic corals are an interesting model with which to study the complexities and evolution of the metazoan circadian clock. We also provide evidence of why the chronobiology of corals is fundamental and extremely important for explaining the biology, physiology, and metabolism of coral reefs. A deeper understanding of these complex issues can help explain coral mass spawning, one of the earth's greatest and most mysterious behavioral phenomena.