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Summary: Coral thermal bleaching resilience can be improved by enhancing photosymbiont thermal tolerance via experimental evolution. While successful for some strains, selection under stable temperatures was ineffective at increasing the thermal threshold of an already thermo‐tolerant photosymbiont (Durusdinium trenchii). Corals from environments with fluctuating temperatures tend to have comparatively high heat tolerance. Therefore, we investigated whether exposure to temperature oscillations can raise the upper thermal limit of D. trenchii.We exposed a D. trenchii strain to stable and fluctuating temperature profiles, which varied in oscillation frequency. After 2.1 yr (54–73 generations), we characterised the adaptive responses under the various experimental evolution treatments by constructing thermal performance curves of growth from 21 to 31°C for the heat‐evolved and wild‐type lineages. Additionally, the accumulation of extracellular reactive oxygen species, photophysiology, photosynthesis and respiration rates were assessed under increasing temperatures.Of the fluctuating temperature profiles investigated, selection under the most frequent oscillations (diurnal) induced the greatest widening of D. trenchii's thermal niche. Continuous selection under elevated temperatures induced the only increase in thermal optimum and a degree of generalism.Our findings demonstrate how differing levels of thermal homogeneity during selection drive unique adaptive responses to heat in a coral photosymbiont. [ABSTRACT FROM AUTHOR]

The thermal tolerance of symbiodiniacean photo-endosymbionts largely underpins the thermal bleaching resilience of their cnidarian hosts such as corals and the coral model Exaiptasia diaphana. While variation in thermal tolerance between species is well documented, variation between conspecific strains is understudied. We compared the thermal tolerance of three closely related strains of Breviolum minutum represented by two internal transcribed spacer region 2 profiles (one strain B1–B1o–B1g–B1p and the other two strains B1–B1a–B1b–B1g) and differences in photochemical and non-photochemical quenching, de-epoxidation state of photopigments, and accumulation of reactive oxygen species under rapid short-term cumulative temperature stress (26–40 °C). We found that B. minutum strains employ distinct photoprotective strategies, resulting in different upper thermal tolerances. We provide evidence for previously unknown interdependencies between thermal tolerance traits and photoprotective mechanisms that include a delicate balancing of excitation energy and its dissipation through fast relaxing and state transition components of non-photochemical quenching. The more thermally tolerant B. minutum strain (B1–B1o–B1g–B1p) exhibited an enhanced de-epoxidation that is strongly linked to the thylakoid membrane melting point and possibly membrane rigidification minimizing oxidative damage. This study provides an in-depth understanding of photoprotective mechanisms underpinning thermal tolerance in closely related strains of B. minutum. [ABSTRACT FROM AUTHOR]

Endosymbiotic dinoflagellates (Symbiodiniaceae) influence coral thermal tolerance at both local and regional scales. In isolation, the effects of host genetics, environment, and thermal disturbances on symbiont communities are well understood, yet their combined effects remain poorly resolved. Here, we investigate Symbiodiniaceae across 1300 km in Australia's Coral Sea Marine Park to disentangle these interactive effects. We identified Symbiodiniaceae to species‐level resolution for three coral species (Acropora cf humilis, Pocillopora verrucosa, and Pocillopora meandrina) by sequencing two genetic markers of the symbiont (ITS2 and psbAncr), paired with genotype‐by‐sequencing of the coral host (DArT‐seq). Our samples predominantly returned sequences from the genus Cladocopium, where Acropora cf humilis affiliated with C3k, Pocillopora verrucosa with C. pacificum, and Pocillopora meandrina with C. latusorum. Multivariate analyses revealed that Acropora symbionts were driven strongly by local environment and thermal disturbances. In contrast, Pocillopora symbiont communities were both partitioned 2.5‐fold more by host genetic structure than by environmental structure. Among the two Pocillopora species, the effects of environment and host genetics explained four times more variation in symbionts for P. meandrina than P. verrucosa. The concurrent bleaching event in 2020 had variable impacts on symbiont communities, consistent with patterns in P. verrucosa and A. cf humilis, but not P. meandrina. Our findings demonstrate how symbiont macroscale community structure responses to environmental gradients depend on host species and their respective population structure. Integrating host, symbiont, and environmental data will help forecast the adaptive potential of corals and their symbionts amidst a rapidly changing environment. [ABSTRACT FROM AUTHOR]

It is widely acknowledged that temperature stress affects an organism's sensitivity to ocean acidification and vice versa, yet it is not clear how the two are mechanistically linked. Here, we induced thermal stress in two coral species with differing bleaching susceptibilities to measure how a reduction in photosynthetic performance impacts intracellular pH ([pH.sub.i]) regulation in the symbiotic dinoflagellates (Symbiodinium sp.) and their host coral cells. Our hypothesis was that thermally induced photosynthetic dysfunction in the symbiont would prevent the efficient removal of additional C[O.sub.2], lowering its buffering capacity and thus increasing the host cell's susceptibility to intracellular acidosis. To test this, we exposed Pocillopora damicornis (a thermally sensitive coral) and Montipora capitata (a thermally resilient coral) to four different temperature treatments (23.8, 25.5, 28 and 31°C) for 1 week. We then isolated intact symbiotic coral endodermal cells, placed them in a live-cell chamber attached to a confocal microscope and bathed them in C[O.sub.2]-acidified seawater (~pH 7.6) for 30 min, before measuring the light-adapted [pH.sub.i] of both the host cell and its symbiont. Cells isolated from P. damicornis were more prone to cellular acidosis (declines in [pH.sub.i] of 11 and 8 % in host and symbiont, respectively, at 31°C relative to 23.8°C) than cells isolated from M. capitata (5 and 4 %, respectively). These results highlight the important role of Symbiodinium productivity (in addition to a range of physico-chemical factors such as skeletal morphology and tissue pigmentation) in determining the sensitivity of corals to rising sea surface temperatures and ocean acidification., Introduction Post-industrial atmospheric C[O.sub.2] levels are increasing at a rate and magnitude that is unparalleled in recent geological history. To date this has resulted in a 1-2°C increase in the [...]

We measured the relationship between symbiont diversity, nutritional potential, and symbiotic success in the cnidarian-dinoflagellate symbiosis, by infecting aposymbiotic (i.e. symbiont-free) specimens of the model sea anemone Aiptasia sp. with a range of Symbiodinium types. Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal's respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host-symbiont interactions may contribute to the host-symbiont specificity seen in cnidarian-dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism., Introduction Cnidarian-dinoflagellate symbioses are widespread in the marine environment and are of great ecological importance (Furla et al. 2005). The symbiosis between anthozoan cnidarians (e.g. corals and sea anemones) and [...]

Among the most successful microeukaryotes to form mutualisms with animals are dinoflagellates in the family Symbiodiniaceae. These photosynthetic symbioses drive significant primary production and are responsible for the formation of coral reef ecosystems but are particularly sensitive when environmental conditions become extreme. Annual episodes of widespread coral bleaching (disassociation of the mutualistic partnership) and mortality are forecasted from the year 2060 under current trends of ocean warming. However, host cnidarians and dinoflagellate symbionts display exceptional genetic and functional diversity, and meaningful predictions of the future that embrace this biological complexity are difficult to make. A recent move to trait-based biology (and an understanding of how traits are shaped by the environment) has been adopted to move past this problem. The aim of this review is to: (1) provide an overview of the major cnidarian lineages that are symbiotic with Symbiodiniaceae; (2) summarise the symbiodiniacean genera associated with cnidarians with reference to recent changes in taxonomy and systematics; (3) examine the knowledge gaps in Symbiodiniaceae life history from a trait-based perspective; (4) review Symbiodiniaceae trait variation along three abiotic gradients (light, nutrients, and temperature); and (5) provide recommendations for future research of Symbiodiniaceae traits. We anticipate that a detailed understanding of traits will further reveal basic knowledge of the evolution and functional diversity of these mutualisms, as well as enhance future efforts to model stability and change in ecosystems dependent on cnidarian-dinoflagellate organisms. [ABSTRACT FROM AUTHOR]

The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including 'temperate–A', AI, Phylotype A´ (A-prime) and 'Mediterranean A', is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized 'yellow cells' as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae. HIGHLIGHTS A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians. The work highlights how animal–algal mutualisms are evolved to thrive under a broad range of environmental conditions. [ABSTRACT FROM AUTHOR]

Dinoflagellates of the family Symbiodiniaceae form mutualistic symbioses with marine invertebrates such as reef‐building corals, but also inhabit reef environments as free‐living cells. Most coral species acquire Symbiodiniaceae horizontally from the surrounding environment during the larval and/or recruitment phase, however the phylogenetic diversity and ecology of free‐living Symbiodiniaceae on coral reefs is largely unknown. We coupled environmental DNA sequencing and genus‐specific qPCR to resolve the community structure and cell abundances of free‐living Symbiodiniaceae in the water column, sediment, and macroalgae and compared these to coral symbionts. Sampling was conducted at two time points, one of which coincided with the annual coral spawning event when recombination between hosts and free‐living Symbiodiniaceae is assumed to be critical. Amplicons of the internal transcribed spacer (ITS2) region were assigned to 12 of the 15 Symbiodiniaceae genera or genera‐equivalent lineages. Community compositions were separated by habitat, with water samples containing a high proportion of sequences corresponding to coral symbionts of the genus Cladocopium, potentially as a result of cell expulsion from in hospite populations. Sediment‐associated Symbiodiniaceae communities were distinct, potentially due to the presence of exclusively free‐living species. Intriguingly, macroalgal surfaces displayed the highest cell abundances of Symbiodiniaceae, suggesting a key role for macroalgae in ensuring the ecological success of corals through maintenance of a continuum between environmental and symbiotic populations of Symbiodiniaceae. [ABSTRACT FROM AUTHOR]

Dinoflagellates within the genus Symbiodinium are photosymbionts of many tropical reef invertebrates, including corals, making them central to the health of coral reefs. Symbiodinium have therefore gained significant research attention, though studies have been constrained by technical limitations. In particular, the generation of viable cells with their cell walls removed (termed protoplasts) has enabled a wide range of experimental techniques for bacteria, fungi, plants, and algae such as ultrastructure studies, virus infection studies, patch clamping, genetic transformation, and protoplast fusion. However, previous studies have struggled to remove the cell walls from armored dinoflagellates, potentially due to the internal placement of their cell walls. Here, we produce the first Symbiodinium protoplasts from three genetically and physiologically distinct strains via incubation with cellulase and osmotic agents. Digestion of the cell walls was verified by a lack of Calcofluor White fluorescence signal and by cell swelling in hypotonic culture medium. Fused protoplasts were also observed, motivating future investigation into intra- and inter-specific somatic hybridization of Symbiodinium. Following digestion and transfer to regeneration medium, protoplasts remained photosynthetically active, regrew cell walls, regained motility, and entered exponential growth. Generation of Symbiodinium protoplasts opens exciting, new avenues for researching these crucial symbiotic dinoflagellates, including genetic modification. [ABSTRACT FROM AUTHOR]

Interspecific hybridisation increases genetic diversity and has played a significant role in the evolution of corals in the genus Acropora. In vitro fertilisation can be used to increase the frequency of hybridisation among corals, potentially enhancing their ability to adapt to climate change. Here, we assessed the field performance of hybrids derived from the highly cross-fertile coral species Acropora sarmentosa and Acropora florida from the Great Barrier Reef. Following outplanting to an inshore reef environment, the 10-month survivorship of the hybrid offspring groups was intermediate between that of the purebred groups, although not all pairwise comparisons were statistically significant. The A. florida purebreds, which had the lowest survivorship, were significantly larger at 10 months post-deployment compared to the other three groups. The four offspring groups harboured the same intracellular photosymbiont communities (Symbiodiniaceae), indicating that observed performance differences were due to the coral host and not photosymbiont communities. The limited differences in the performance of the groups and the lack of outbreeding depression of the F1 hybrids in the field suggest that interspecific hybridisation may be a useful method to boost the genetic diversity, and as such increase the adaptive capacity, of coral stock for restoration of degraded and potentially genetically eroded populations., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

The heat tolerance of corals is largely determined by their microbial photosymbionts (Symbiodiniaceae, colloquially known as zooxanthellae). Therefore, manipulating symbiont communities may enhance the ability of corals to survive summer heatwaves. Although heat-tolerant and -sensitive symbiont species occur in nature, even corals that harbour naturally tolerant symbionts have been observed to bleach during summer heatwaves. Experimental evolution (i.e., laboratory selection) of Symbiodiniaceae cultures under elevated temperatures has been successfully used to enhance their upper thermal tolerance, both in vitro and, in some instances, following their reintroduction into corals. In this review, we present the state of this intervention and its potential role within coral reef restoration, and discuss the next critical steps required to bridge the gap to implementation., Competing Interests: Declaration of interests None declared by authors., (Crown Copyright © 2024. Published by Elsevier Ltd. All rights reserved.)