Endosymbiotic Algae Research Articles

Toward the generation of pure coral genomes with experimental and bioinformatic improvements

Stony corals, the primary architects of coral reef ecosystems, are largely underrepresented in omics studies despite their importance. The presence of endosymbiotic Symbiodiniaceae algae complicates the extraction of pure coral DNA, posing a challenge for genomic research. Here, we devised a comprehensive methodological framework that incorporates various experimental treatments to achieve 99% purity in coral DNA extraction and a robust bioinformatics pipeline to guarantee the assembly of high-quality, contamination-free coral genomes. Validation of our framework using Acropora millepora samples demonstrated its efficacy and superiority in obtaining high-quality pure coral genomes using easily accessible adult colony. This integrated framework serves as a critical foundation for large-scale genome-enabled research on stony corals, providing insight into coral evolution and conservation.

Low-CO2-inducible bestrophins outside the pyrenoid sustain high photosynthetic efficacy in diatoms.

Anion transporters sustain a variety of physiological states in cells. Bestrophins (BSTs) belong to a Cl- and/or HCO3- transporter family conserved in bacteria, animals, algae, and plants. Recently, putative BSTs were found in the green alga Chlamydomonas reinhardtii, where they are upregulated under low CO2 (LC) conditions and play an essential role in the CO2-concentrating mechanism (CCM). The putative BST orthologs are also conserved in diatoms, secondary endosymbiotic algae harboring red-type plastids, but their physiological functions are unknown. Here, we characterized the subcellular localization and expression profile of BSTs in the marine diatoms Phaeodactylum tricornutum (PtBST1 to 4) and Thalassiosira pseudonana (TpBST1 and 2). PtBST1, PtBST2, and PtBST4 were localized at the stroma thylakoid membrane outside of the pyrenoid, and PtBST3 was localized in the pyrenoid. Contrarily, TpBST1 and TpBST2 were both localized in the pyrenoid. These BST proteins accumulated in cells grown in LC but not in 1% CO2 (high CO2 [HC]). To assess the physiological functions, we generated knockout mutants for the PtBST1 gene by genome editing. The lack of PtBST1 decreased photosynthetic affinity for dissolved inorganic carbon to the level comparable with the HC-grown wild type. Furthermore, non-photochemical quenching in LC-grown cells was 1.5 to 2.0 times higher in the mutants than in the wild type. These data suggest that HCO3- transport at the stroma thylakoid membranes by PtBST1 is a critical part of the CO2-evolving machinery of the pyrenoid in the fully induced CCM and that PtBST1 may modulate photoprotection under CO2-limited environments in P. tricornutum.

Response of two temperate scleractinian corals to projected ocean warming and marine heatwaves.

The Mediterranean Sea is a hotspot of global change, particularly exposed to ocean warming and the increasing occurrence of marine heatwaves (MHWs). However, experiments based on long-term temperature data from the field are scarce. Here, we investigate the response of the zooxanthellate coral Cladocora caespitosa and the azooxanthellate coral Astroides calycularis to future warming and MHWs based on 8 years of in situ data. Corals were maintained in the laboratory for five months under four temperature conditions: Warming (3.2°C above the in situ mean from 2012 to 2020), Heatwave (temperatures of 2018 with two heatwaves), Ambient (in situ mean) and Cool (deeper water temperatures). Under the Warming treatment, some C. caespitosa colonies severely bleached and A. calycularis colonies presented necrosis. Cladocora caespitosa symbiosis was impaired by temperature with a decrease in the density of endosymbiotic algae and an increase in per cent whiteness in all the treatments except for the coolest. Recovery for both species was observed through different mechanisms such as regrowth of polyps of A. calycularis and recovery of pigmentation for C. caespitosa. These results suggest that A. calycularis and C. caespitosa may be resilient to heat stress and can recover from physiological stresses caused by heatwaves in the laboratory.

Effects of Norflurazon and UV Radiation on Symbiotic and Free-Living Hydra

In this study, we aimed to document the freshwater symbiotic interactions along with the impact of the abiotic environment and anthropogenic effects on the functionality of freshwater organisms. Symbiotic green hydra (Z) and free-living brown hydra (S), either separately or both species together, were treated with the herbicide norflurazon in concentrations of 2 × 10−6 mol/L (N6) and 2 × 10−7 mol/L (N7) for 72 h. Also, hydras were treated with both norflurazon and UV radiation at a wavelength of 254 nm for 2 min or were irradiated only. The next part of the experiment was performed in the same way but with added suspensions of isolated endosymbiotic alga, free-living alga, or both algae together. Mortality, migration, tentacle and tissue damage, changes in the thickness of the mesoglea of hydras, and clustering of algae were monitored. Green hydra generally showed lower rates of migration, and mortality was observed only in green hydra exposed to UV radiation. Tentacle damage was more pronounced in green hydra and included a specific fork-like structure. The use of cryofixation and TEM enabled us to partly elucidate the effect of clustering of algae. In summary, our study provides new insights into the influence of different environmental stressors and their combination on symbiotic and free-living freshwater hydras and algae and a better understanding of interactions in freshwater ecosystems.

Phylogenetic affiliation of Pedinomonas noctilucae and green Noctiluca scintillans nutritional dynamics in the Gulf of Mannar, Southeastern Arabian Sea

The present investigation focused on studying the phylogenetic position of the green Noctiluca endosymbiont, Pedinomonas noctilucae, collected from the Gulf of Mannar, India. In this study, we re-examined the evolutionary position of this endosymbiotic algae using rbcL sequences. The phylogenetic analysis revealed that P. noctilucae is distantly related to the Pedinomonas species, and formed a monophyletic clade with Marsupiomandaceae. Based on the phylogenetic association of endosymbiont with Maruspiomonadales it was concluded that the endosymbiont belongs to an independent genus within the family Marsupiomonadaceae. At the site of the bloom, Noctiluca scintillans was found to exhibit a dense monospecific proliferation, with an average cell density of 27.l88 × 103 cells L−1. The investigation revealed that the green Noctiluca during its senescent phase primarily relied on autotrophic nutrition, which was confirmed by the presence of a high number of trophonts, vegetatively reproducing cells (1.45 × 103 cells L−1) and the absence of food vacuoles.

How Daphnia magna Defends Itself against Predators: Mechanisms and Adaptations in a Freshwater Microcosm

The freshwater water flea (Daphnia magna Straus, 1820) is prey for numerous predators. Yet it possesses a wide range of strategies to defend itself against predation. The aim of this work is to investigate the defensive mechanisms employed by D. magna to reduce predation by the coelenterate Hydra viridissima, and two planarians, Polycelis felina and Dugesia gonocephala. To do this, we used a freshwater microcosm. An additional aim is to investigate interactions with the presence of the isolated endosymbiotic algae from green hydra, thus combining and observing the interaction of the zooplankton and microalgal component. Each experiment included five replicates (13.5 °C, 25 °C), in crystallizing glass containers (60 mL volume, 60 mm diameter, 35 mm height), including satiated (fed with larvae of Artemia salina) and starved predators, respectively (one or five individuals of a particular predator species in one microcosm). As the isolated microalgae are unique, we tracked the following three mechanisms of Daphnia defense for the first time including precisely this microalgal component: (i) grouping (visual magnification), i.e., two or more Daphnia holding together; (ii) the phenomenon of overproduction, i.e., any number of Daphnia in one container above the 10 initially added individuals; and (iii) accelerated movement (“bullet movement”), i.e., high-speed movements in particular microcosms. The results provide new information for a better understanding of the interspecific relationships in systems that include both zooplankton and microalgal components.

Globally distributed bacteriophage genomes reveal mechanisms of tripartite phage-bacteria-coral interactions.

Reef-building corals depend on an intricate community of microorganisms for functioning and resilience. The infection of coral-associated bacteria by bacteriophages can modify bacterial ecological interactions, yet very little is known about phage functions in the holobiont. This gap stems from methodological limitations that have prevented the recovery of high-quality viral genomes and bacterial host assignment from coral samples. Here, we introduce a size fractionation approach that increased bacterial and viral recovery in coral metagenomes by 9-fold and 2-fold, respectively, and enabled the assembly and binning of bacterial and viral genomes at relatively low sequencing coverage. We combined these viral genomes with those derived from 677 publicly available metagenomes, viromes, and bacterial isolates from stony corals to build a global coral virus database of over 20,000 viral genomic sequences spanning four viral realms. The tailed bacteriophage families Kyanoviridae and Autographiviridae were the most abundant, replacing groups formerly referred to as Myoviridae and Podoviridae, respectively. Prophage and CRISPR spacer linkages between these viruses and 626 bacterial metagenome-assembled genomes and bacterial isolates showed that most viruses infected Alphaproteobacteria, the most abundant class, and less abundant taxa like Halanaerobiia and Bacteroidia. A host-phage-gene network identified keystone viruses with the genomic capacity to modulate bacterial metabolic pathways and direct molecular interactions with eukaryotic cells. This study reveals the genomic basis of nested symbioses between bacteriophage, bacteria, and the coral host and its endosymbiotic algae.

Complex Endosymbioses I: From Primary to Complex Plastids, Serial Endosymbiotic Events.

A considerable part of the diversity of eukaryotic phototrophs consists of algae with plastids that evolved from endosymbioses between two eukaryotes. These complex plastids are characterized by a high number of envelope membranes (more than two) and some of them contain a residual nucleus of the endosymbiotic alga called a nucleomorph. Complex plastid-bearing algae are thus chimeric cell assemblies, eukaryotic symbionts living in a eukaryotic host. In contrast, the primary plastids of the Archaeplastida (plants, green algae, red algae, and glaucophytes) possibly evolved from a single endosymbiosis with a cyanobacterium and are surrounded by two membranes. Complex plastids have been acquired several times by unrelated groups of eukaryotic heterotrophic hosts, suggesting that complex plastids are somewhat easier to obtain than primary plastids. Evidence suggests that complex plastids arose twice independently in the green lineage (euglenophytes and chlorarachniophytes) through secondary endosymbiosis, and four times in the red lineage, first through secondary endosymbiosis in cryptophytes, then by higher-order events in stramenopiles, alveolates, and haptophytes. Engulfment of primary and complex plastid-containing algae by eukaryotic hosts (secondary, tertiary, and higher-order endosymbioses) is also responsible for numerous plastid replacements in dinoflagellates. Plastid endosymbiosis is accompanied by massive gene transfer from the endosymbiont to the host nucleus and cell adaptation of both endosymbiotic partners, which is related to the trophic switch to phototrophy and loss of autonomy of the endosymbiont. Such a process is essential for the metabolic integration and division control of the endosymbiont in the host. Although photosynthesis is the main advantage of acquiring plastids, loss of photosynthesis often occurs in algae with complex plastids. This chapter summarizes the essential knowledge of the acquisition, evolution, and function of complex plastids.

Viral Chemotaxis of Paramecium Bursaria Altered by Algal Endosymbionts.

Chemotaxis is widespread across many taxa and often aids resource acquisition or predator avoidance. Species interactions can modify the degree of movement facilitated by chemotaxis. In this study, we investigated the influence of symbionts on Paramecium bursaria's chemotactic behavior toward chloroviruses. To achieve this, we performed choice experiments using chlorovirus and control candidate attractors (virus stabilization buffer and pond water). We quantified the movement of Paramecia grown with or without algal and viral symbionts toward each attractor. All Paramecia showed some chemotaxis toward viruses, but cells without algae and viruses showed the most movement toward viruses. Thus, the endosymbiotic algae (zoochlorellae) appeared to alter the movement of Paramecia toward chloroviruses, but it was not clear that ectosymbiotic viruses (chlorovirus) also had this effect. The change in behavior was consistent with a change in swimming speed, but a change in attraction remains possible. The potential costs and benefits of chemotactic movement toward chloroviruses for either the Paramecia hosts or its symbionts remain unclear.

Environmental pH signals the release of monosaccharides from cell wall in coral symbiotic alga.

Reef-building corals thrive in oligotrophic environments due to their possession of endosymbiotic algae. Confined to the low pH interior of the symbiosome within the cell, the algal symbiont provides the coral host with photosynthetically fixed carbon. However, it remains unknown how carbon is released from the algal symbiont for uptake by the host. Here we show, using cultured symbiotic dinoflagellate, Breviolum sp., that decreases in pH directly accelerates the release of monosaccharides, that is, glucose and galactose, into the ambient environment. Under low pH conditions, the cell surface structures were deformed and genes related to cellulase were significantly upregulated in Breviolum. Importantly, the release of monosaccharides was suppressed by the cellulase inhibitor, glucopyranoside, linking the release of carbon to degradation of the agal cell wall. Our results suggest that the low pH signals the cellulase-mediated release of monosaccharides from the algal cell wall as an environmental response in coral reef ecosystems.

The roles of heating rate, intensity, and duration on the response of corals and their endosymbiotic algae to thermal stress

Anthropogenic ocean warming is one of the biggest threats to marine organisms worldwide. However, it remains unclear how the duration and intensity of thermal anomalies affect organismal stress responses and thermal thresholds. We used detailed tracking of coral endosymbiont and host physiology and dose-response analyses to compare the effects of multiple heating rates, intensities, and exposure durations on two reef-building corals, Acropora hemprichii and Porites lobata, from adjacent sides of a reef (protected vs. exposed) in the Central Red Sea known to differ in high-frequency (< 24 h) temperature variability. Corals were exposed to acute heat exposures (18 h) with four target temperatures (32 °C, 35 °C, 36.5 °C, and 38 °C), versus prolonged heat exposures lasting 7–15 days where temperatures were raised 0.5 and 1.5 °C day−1 to four target temperatures (32 °C, 33.5 °C, 35 °C, and 36.5 °C). In the prolonged experiment, dose-response curves assessing algal endosymbiont Fv/Fm revealed little initial effect of temperature, before an exponential decline above 34 °C for both species. Temperature at time of measurement and degree heating hours above 34 °C (DHH34) were the variables most strongly associated with declines in Fv/Fm. The Fv/Fm thermal thresholds for P. lobata from the high-variability protected site were higher than the exposed site in the faster heating, prolonged heat stress experiment despite minimal differences in endosymbiont density, chlorophyll-a, and host protein between sites. Together, our dose-response analysis revealed complex effects of DHH34, heating rate, and species-specific differences in the influence of local thermal histories shaping thermotolerance limits for these corals.

Algal symbionts of the freshwater sponge Ephydatia muelleri

The freshwater sponge, Ephydatia muelleri, is an emerging model system for studying animal:microbe symbioses. Intracellular green microalgae are one of the more common symbionts that live in a facultative mutualism with E. muelleri. While these symbioses have long been known, the identity of the algal symbionts in E. muelleri cells has not been studied in detail. Here, we isolate and characterize endosymbiotic algae from E. muelleri collected from different geographic locations. We find that the algae can be transmitted through asexually produced gemmules and importantly that they can form symbioses with different, differentiated sponge cell types in the adult sponge. Our findings indicate that at least two algal lineages form endosymbioses with E. muelleri. One of the lineages includes species commonly found in samples from two locations in Canada and one in the United States (clade 1: closely related to Auxenochlorella pyrenoidosa). The other clade includes algae found in sponges from one site in Maine, USA, and Lewiniosphaera symbiontica, which is a strain isolated in 1956 from the freshwater sponge Spongilla. We compared microbiomes found in cultures of microalgae as well as the original sponge hosts, and found that very similar bacterial microbiomes associate with both clades (91 orders of Bacteria are shared among the samples we compared). The microbiomes found in the cultures resemble, with a high degree of overlap, the microbiome associated with the sponge host.

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species under simulated future conditions of ocean warming and acidification

The symbiotic relationship between coral and its endosymbiotic algae, Symbiodiniaceae, greatly influences the hosts’ potential to withstand environmental stress. To date, the effects of climate change on this relationship has primarily focused on adult corals. Uncovering the effects of environmental stress on the establishment and development of this symbiosis in early life stages is critical for predicting how corals may respond to climate change. To determine the impacts of future climate projections on the establishment of symbionts in juvenile corals, ITS2 amplicon sequencing of single coral juveniles was applied to Goniastrea retiformis and Acropora millepora before and after exposure to three climate conditions of varying temperature and pCO2 levels (current and RCP8.5 in 2050 and 2100). Compared to ambient conditions, juvenile corals experienced shuffling in the relative abundance of Cladocopium (C1m, decrease) to Durusdinium (D1 and D1a, increase) over time. We calculated a novel risk metric incorporating functional redundancy and likelihood of impact on host physiology to identify the loss of D1a as a “low risk” to the coral compared to the loss of “higher risk” taxa like D1 and C1m. Although the increase in stress tolerant Durusdinium under future warming was encouraging for A. millepora, by 2100, G. retiformis communities displayed signs of symbiosis de-regulation, suggesting this acclimatory mechanism may have species-specific thresholds. Whilst this study cannot specifically disentangle the individual effects of temperature and pCO2, it does provide valuable insights into the impacts of both stressors combined. These results emphasize the need for understanding of long-term effects of climate change induced stress on coral juveniles, and their potential for increased acclimation to heat tolerance through changes in symbiosis.

Potential role of N6-adenine DNA methylation in alternative splicing and endosymbiosis in Paramecium bursaria

N6-adenine DNA methylation (6mA), a rediscovered epigenetic mark in eukaryotic organisms, diversifies in abundance, distribution, and function across species, necessitating its study in more taxa. Paramecium bursaria is a typical model organism with endosymbiotic algae of the species Chlorella variabilis. This consortium therefore serves as a valuable system to investigate the functional role of 6mA in endosymbiosis, as well as the evolutionary importance of 6mA among eukaryotes. In this study, we report the first genome-wide, base pair-resolution map of 6mA in P.bursaria and identify its methyltransferase PbAMT1. Functionally, 6mA exhibits a bimodal distribution at the 5' end of RNA polymerase II-transcribed genes and possibly participates in transcription by facilitating alternative splicing. Evolutionarily, 6mA co-evolves with gene age and likely serves as a reverse mark of endosymbiosis-related genes. Our results offer new insights for the functional diversification of 6mA in eukaryotes as an important epigenetic mark.

From the shallow to the mesophotic: a characterization of Symbiodiniaceae diversity in the Red Sea NEOM region

IntroductionThe northern Red Sea has been coined a refuge for reef corals due to the exceptional thermal tolerance of these organisms. With ocean warming threatening coral reefs worldwide, a panoptic characterization of corals living in extreme conditions may provide insights into future responses of corals to environmental change. Among other factors, the genotype of the endosymbiotic algae in the family Symbiodiniaceae has been shown to have major implications on the distribution and resilience of their coral hosts. In this study, we aim at genotyping the Symbiodiniaceae communities associated with three depth generalist and one depth specialist coral species, characterized by the ability to withstand environmental conditions that are apparently limiting for other corals and occurring in a unique geographical region.MethodsWe sampled 50 corals from the northern Saudi Arabian Red Sea and the Gulf of Aqaba, covering a 97 m bathymetric gradient. We used high-throughput ITS2 gene sequencing and recovered different patterns of host–algal associations.Results and discussionThe majority of the recovered algal genotypes appeared host- and environment-specific, while others were more widely distributed. At large, coral specimens were overwhelmingly associated with symbionts from the genus Cladocopium and specifically with many previously undescribed genotypes. This suggests the selection of specific genotypes, which might confer resistance and/or resilience to their host counterparts. Interestingly, we found a limited association with Durusdinium spp. and other known tolerant taxa in mesophotic corals in the northern Red Sea, but not in the Gulf of Aqaba. The broad absence of Durusdinium spp., typically ascribed to be stress tolerant, warrants further investigation into Symbiodiniaceae species that convey environmental resilience. Our data will serve as a baseline to explore the occurrence of specific symbionts that might be contributing to coral acclimation and adaptation and to assay how biodiversity might be impacted if subjected to increasing stressors.

Modeling food dependent symbiosis in Exaiptasia pallida

Cnidaria, marine invertebrates that include reef-building stony corals, often rely on photosynthetic endosymbionts to obtain the energy they need for growth. Increased temperatures and/or nutrient pollution can disrupt mutualistic properties of the symbiosis, leading to host mortality. However, the precise mechanism by which this dysbiosis occurs is still unclear. Sea anemones, other cnidarians that may host algal endosymbionts, are used as a model organism for the coral holobiont to understand the costs and benefits of symbionts, but the exact nature of the costs of symbionts on the hosts is still unclear. Here we developed a Dynamic Energy Budget (DEB) model and fit the model to data from the anemone Exaiptasia pallida and its endosymbiotic algae, Breviolum minutum, in order to identify the most likely mechanism of symbiont costs. In order to match the laboratory dataset, our model needed an explicit symbiont demand term, in which the symbiont can “consume” host tissue to forcibly extract nitrogen. The model demonstrates the role of the symbiont as an amplifier of the host’s state: a growing anemone grows better with symbionts, while a malnourished anemone looses biomass faster with a symbiont than without. This model allows us to project Cnidaria holobiont growth as a function of environmental conditions and adds a new framework for which to capture the direct cost a symbiont has on Cnidaria hosts.

Diversity and composition of bacterial communities associated with healthy and bleached coral Fungia sp. in Nha Trang bay, Vietnam

Coral bleaching is probably caused by the loss of endosymbiotic algae from the host tissue or disturbance of the microbial community composition of corals. In particular, bacteria inhabiting the surface mucus layer of corals are supposed to mediate coral health, but their role in coral bleaching has not been fully clarified. In the present study, we collected mucus samples from bleached and healthy Fungia sp. colonies in Nha Trang bay to investigate biodiversity and bacterial community composition using 16S rRNA gene amplicon next-generation sequencing. The results indicated rich biodiversity and significant changes in bacterial communities between bleached and healthy corals. Two phyla, Proteobacteria and Bacteroidetes, making up approximately 80% of the total bacterial abundance, were predominant in both bleached and healthy samples. Three phyla, Actinobacteria, Planctomycetes, and Cyanobacteria identified as minor taxa, were low in abundance in both samples. However, there were significant differences in bacterial communities at the genus level. Three bacterial genera, Erythobacteria, Synechcococcus CC9902, and Candidatus Actinomarina, involved in coral health protection, were mostly determined in the healthy coral samples. Whereas, five genera, Algicola, Fusibacter, Halodesulfovibrio, Marinifilum, and especially the genus Vibrio, were mainly detected in the bleached corals with a notable increase in relative abundance. Moreover, analysis of alpha and beta diversity (NMDS) also confirmed that there were significant changes in bacterial composition between the bleached and healthy corals (p-value &lt;0.05). These findings suggest that the disturbance of the bacterial community composition living on coral is one of the factors causing coral bleaching, beside environmental factors like pH, temperature, and dissolved oxygen.

Antiscalants used in the desalination industry impact the physiology of the coral Montipora capricornis

Many coral reefs are found in arid and semi-arid regions that often face severe water scarcity and depend on seawater desalination for freshwater supply. Alongside freshwater production, desalination plants discharge brine waste into the sea. Brine includes various chemicals (e.g., antiscalants) that may harm the coastal environment. Although widely used, little is known about the ecotoxicological effects of antiscalants (AS) on hard corals. This study compared the impacts of polyphosphonate-based and polymer-based ASs on the coral Montipora capricornis. After two weeks of exposure, we determined the effects of AS on coral physiology, symbiotic microalgae, and associated bacteria, using various analytical approaches such as optical coherence tomography, pulse amplitude modulated fluorometry, and oxidative stress biomarkers. Both ASs reduced polyp activity (∼25%) and caused tissue damage (30% and 41% for polymer and polyphosphonate based AS, respectively). In addition, exposure to polyphosphonate-based AS decreased the abundance of endosymbiotic algae (39%) and upregulated the antioxidant capacity of the animal host (45%). The microalgal symbionts were under oxidative stress, with increased levels of antioxidant capacity and oxidative damage (a 2-fold increase compared to the control). Interestingly, exposure to AS enhanced the numbers of associated bacteria (∼40% compared to the control seawater) regardless of the AS type. Our results introduce new insights into the effects of brine on the physiology of hard corals, highlighting that choosing AS type must be examined according to the receiving ecosystem.

Declining metal availability in the Mesozoic seawater reflected in phytoplankton succession

Variable trace metal concentrations in the Precambrian ocean were closely linked to oxygen availability, although less is known about the drivers of seawater trace metal chemistry after the spread of complex life into the Phanerozoic eon. A major phytoplankton succession took place at the transition from the Palaeozoic to the Mesozoic era (~250 Myr ago), from an ocean dominated by the green Archaeplastida to secondary endosymbiotic algae with red-algal-derived plastids. Here, our comparative genomic analysis of 26 complete proteomes and metal domain analysis of additional 608 partially complete sequences of phytoplankton reveal that groups with different evolutionary history have distinct metal-binding proteins and contrasting metal acquisition strategies, adapted to differing availability of trace metals. The secondary-endosymbiont-bearing lineages are better adapted to well-oxygenated, nutrient-poor environments. This is supported by an enhanced thiol-based binding affinity of their transporters, coupled with minimized proteomic requirement for trace elements such as iron, copper and zinc at both protein and domain levels. Such different metal requirements across these lineages suggest a drastic decline in open-ocean trace metal concentrations at the inception of the Mesozoic, contributing to the shifts in phytoplankton communities that drove major changes in ocean chemical buffering.

Cryptic diversity and spatial genetic variation in the coral Acropora tenuis and its endosymbionts across the Great Barrier Reef.

Genomic studies are uncovering extensive cryptic diversity within reef-building corals, suggesting that evolutionarily and ecologically relevant diversity is highly underestimated in the very organisms that structure coral reefs. Furthermore, endosymbiotic algae within coral host species can confer adaptive responses to environmental stress and may represent additional axes of coral genetic variation that are not constrained by taxonomic divergence of the cnidarian host. Here, we examine genetic variation in a common and widespread, reef-building coral, Acropora tenuis, and its associated endosymbiotic algae along the entire expanse of the Great Barrier Reef (GBR). We use SNPs derived from genome-wide sequencing to characterize the cnidarian coral host and organelles from zooxanthellate endosymbionts (genus Cladocopium). We discover three distinct and sympatric genetic clusters of coral hosts, whose distributions appear associated with latitude and inshore-offshore reef position. Demographic modelling suggests that the divergence history of the three distinct host taxa ranges from 0.5 to 1.5million years ago, preceding the GBR's formation, and has been characterized by low-to-moderate ongoing inter-taxon gene flow, consistent with occasional hybridization and introgression typifying coral evolution. Despite this differentiation in the cnidarian host, A.tenuis taxa share a common symbiont pool, dominated by the genus Cladocopium (Clade C). Cladocopium plastid diversity is not strongly associated with host identity but varies with reef location relative to shore: inshore colonies contain lower symbiont diversity on average but have greater differences between colonies as compared with symbiont communities from offshore colonies. Spatial genetic patterns of symbiont communities could reflect local selective pressures maintaining coral holobiont differentiation across an inshore-offshore environmental gradient. The strong influence of environment (but not host identity) on symbiont community composition supports the notion that symbiont community composition responds to habitat and may assist in the adaptation of corals to future environmental change.