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Diatoms, dinoflagellates, and coccolithophores are dominant groups of marine eukaryotic phytoplankton that are collectively responsible for the majority of primary production in the ocean.1 These phytoplankton contain additional intracellular membranes around their chloroplasts, which are derived from ancestral engulfment of red microalgae by unicellular heterotrophic eukaryotes that led to secondary and tertiary endosymbiosis.2 However, the selectable evolutionary advantage of these membranes and the physiological significance for extant phytoplankton remain poorly understood. Since intracellular digestive vacuoles are ubiquitously acidified by V-type H+-ATPase (VHA),3 proton pumps were proposed to acidify the microenvironment around secondary chloroplasts to promote the dehydration of dissolved inorganic carbon (DIC) into CO2, thus enhancing photosynthesis.4,5 We report that VHA is localized around the chloroplasts of centric diatoms and that VHA significantly contributes to their photosynthesis across a wide range of oceanic irradiances. Similar results in a pennate diatom, dinoflagellate, and coccolithophore, but not green or red microalgae, imply the co-option of phagocytic VHA activity into a carbon-concentrating mechanism (CCM) is common to secondary endosymbiotic phytoplankton. Furthermore, analogous mechanisms in extant photosymbiotic marine invertebrates6,7,8 provide functional evidence for an adaptive advantage throughout the transition from endosymbiosis to symbiogenesis. Based on the contribution of diatoms to ocean biogeochemical cycles, VHA-mediated enhancement of photosynthesis contributes at least 3.5 Gtons of fixed carbon per year (or 7% of primary production in the ocean), providing an example of a symbiosis-derived evolutionary innovation with global environmental implications.

The precise mechanisms that allow animals and phototrophic organisms to form a stable photosymbiotic relationship are still unknown. While previous studies focused on genomic adaptations of the animal host, more recent research looked into the role of bacteria in photosymbiosis. Here, we analyzed the core microbiome of the sea slug Berghia stephanieae and its food source Exaiptasia diaphana to understand if the microbiome and the linked bacterial metabolic pathways differ between unstable and stable photosymbiosis. This sea slug feeds solely on the model cnidarian E. diaphana and steals their photobionts which the slug can only maintain for a week. We additionally examined the influence of light and starvation stress on the slug's bacterial composition, which are common experimental set-ups to elucidate the photosymbiotic relationship in the slugs. Our results show that the core microbiome of B. stephanieae and E. diaphana differed significantly suggesting that the slug's microbiome is not obtained from its food source or the water column and indicates a vertical transmission. Further, differences in metabolic pathways imply that the microbiome of B. stephanieae does not support a stable photosymbiosis due to an insufficient nitrogen cycle on part of the photobiont. Starving the slugs induced a shift towards an increased abundance of potential pathogens and led to a downregulation in the sulphur cycle. Yet, starvation in darkness resulted in the depletion of most bacteria and induced a metabolic switch toward bacterial nitrogen fixation. This emphasizes that different holobiont members contribute to essential nutrient cycles, and it is important to look beyond the photobiont to understand the sea slug holobiont. [ABSTRACT FROM AUTHOR]

Photosymbioses between heterotrophic hosts and autotrophic symbionts are evolutionarily prevalent and ecologically significant. However, the molecular mechanisms behind such symbioses remain less elucidated, which hinders our understanding of their origin and adaptive evolution. This study compared gene expression patterns in a photosymbiotic bivalve (Fragum sueziense) and a closely related non-symbiotic species (Trigoniocardia granifera) under different light conditions to detect potential molecular pathways involved in mollusc photosymbiosis. We discovered that the presence of algal symbionts greatly impacted host gene expression in symbiont-containing tissues. We found that the host immune functions were suppressed under normal light compared with those in the dark. In addition, we found that cilia in the symbiont-containing tissues play important roles in symbiont regulation or photoreception. Interestingly, many potential photosymbiosis genes could not be annotated or do not exhibit orthologues in T. granifera transcriptomes, indicating unique molecular functions in photosymbiotic bivalves. Overall, we found both novel and known molecular mechanisms involved in animal-algal photosymbiosis within bivalves. Given that many of the molecular pathways are shared among distantly related host lineages, such as molluscs and cnidarians, it indicates that parallel and/or convergent evolution is instrumental in shaping host–symbiont interactions and responses in these organisms. [ABSTRACT FROM AUTHOR]

Abstract Background Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. Results We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching. Conclusions Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract

Photosymbiosis evolved recurrently within the tree of life. Oxygen could have provided the primary selection pressure for photosymbiont acquisition. Host recognition and immunity are involved in photosymbiont maintenance. Intracellular pathogens can trigger photosymbiont maintenance. Genetics will open up the analysis of the cellular mechanisms of photosymbiont maintenance. Oxygenic photosynthesis evolved in cyanobacteria around 3.2 giga-annum (Ga) ago and was acquired by eukaryotes starting around 1.8 Ga ago by endosymbiosis. Photosymbiosis results either from integration of a photosynthetic bacteria by heterotrophic eukaryotes (primary photosymbiosis) or by successive integration of photosymbiotic eukaryotes by heterotrophic eukaryotes (secondary photosymbiosis). Primary endosymbiosis is thought to have been a rare event, whereas secondary and higher-order photosymbiosis evolved multiple times independently in different taxa. Despite its recurrent evolution, the molecular and cellular mechanisms underlying photosymbiosis are unknown. In this opinion, we discuss the primary events leading to the establishment of photosymbiosis, and we present recent research suggesting that, in some cases, domestication occurred instead of symbiosis, and how oxygen and host immunity can be involved in symbiont maintenance. [ABSTRACT FROM AUTHOR]

Numerous marine invertebrates form symbiotic relationships with single-celled algae, termed "photosymbioses", and the diversity of these interactions is likely underestimated. We examined Phidiana lynceus, a cladobranch sea slug that feeds on photosymbiotic hydrozoans. We assessed its ability to acquire/retain algal symbionts by examining specimens in starvation, finding that P. lynceus is able to incorporate and retain symbionts for up to 20 days. Examining body size during starvation revealed that P. lynceus does not receive enough energy from hosting symbionts to maintain its body mass let alone grow. Intact symbionts were still present in deceased specimens, indicating that P. lynceus does not digest all of its symbionts, even when starving to death. We also examined slug behavior in the field and lab to determine if it seeks light to facilitate photosynthesis, which could provide energetic and oxygenic benefits. In the field, slugs were always observed hiding under stones during the day and they displayed light avoidance in the lab, suggesting this species actively prevents photosynthesis and the benefits it could receive. Lastly, we measured their metabolic rates during the day and night and when treated with and without a photosynthetic inhibitor. Higher metabolic rates at night indicate that this species displays nocturnal tendencies, expending more energy when it emerges at night to forage. Paradoxically, P. lynceus has evolved all of the requisite adaptations to profit from photosymbiosis but it chooses to live in the dark instead, calling into question the nature of this symbiosis and what each partner might receive from their interaction. [ABSTRACT FROM AUTHOR]

The matter of photosymbiosis in Paleozoic corals remains unresolved as it is not possible to directly check for the presence of algal symbionts in fossil corals. However, present-day photosymbiotic corals are characterised by a number of features that can be evaluated in fossil corals as well, such as large, highly integrated colonies, growth banding, and platy growth forms in mesophotic conditions. The present study aims to evaluate these features in heliolitid corals. Heliolitids were relatively highly integrated, compared to other Paleozoic corals and could produce large colonies, over 1 m in diameter. In this study, heliolitid corals from different outcrops from the Silurian (~ 444 to 419 ma) of Gotland (Sweden) were analysed, and additional Devonian (~ 419 to 359 ma) specimens from Belgium, Poland and Morocco, featuring cyclic growth banding, were also included. Overall, over 60% of studied specimens from Lower Visby Formation in Ireviken and over 80% from Eke Formation in Lau Käldu are platy or tabular. Those outcrops represent environments that were mesophotic. Specimens from the shallower Upper Visby Formation in Ygne are dominated by branching forms instead. The apparent light-related skeletal plasticity, high colony integration, growth banding, and the absence of heliolitids in deep water environments implies that some of these corals were most likely photosymbiotic. [ABSTRACT FROM AUTHOR]

Symsagittifera roscoffensis forms a photosymbiotic relationship with the alga Tetraselmis convolutae within the intertidal zone. Juveniles lack algal symbionts at birth and acquire them from the environment. Requiring light for photosynthesis, they position themselves within the water column while also balancing the risk of being washed away. To understand their behavioural adaptations, we conducted experiments on their movement in response to algal cues (chemotaxis), light gradients (phototaxis), and mechanical vibrations. Aposymbiotic juveniles showed three times more positive displacement towards algae. Adults exhibited positive phototaxis but retreated from high light intensity. When introduced to a column with a light source, the worms remained just below the surface. In the mechanical vibration experiment, worms only descended when vibrations exceeded a threshold. These findings suggest that S. roscoffensis has chemotactic abilities crucial for acquiring algae and acquires light for photosynthesis while minimizing dispersal risk and photoinhibition, facilitating its life cycle in the intertidal zone. [ABSTRACT FROM AUTHOR]

Three populations of the solar-powered sea slug Elysia crispata on reefs from the southern Gulf of Mexico and the Caribbean were analyzed. The aim was to describe and compare the changes in abundance and size of this species in different localities, as a function of depth and time-of-day. We hypothesized that differences in abundance would be related to locality, time of the day and depth, and differences in size would be related to locality and time of the day. Using snorkeling and SCUBA diving, all individuals within quadrats were counted and measured. A total of 680 organisms were recorded at Verde, Arcas and Puerto Morelos (PM) reefs at five times of the day (sunrise, morning, zenith, evening, and night) and depths of 0–13 m. Zero inflated negative binomial (ZINB) regressions adjusted to abundance data showed that E. crispata in Arcas and Verde reefs is expected to be more abundant (> 50) in shallow depths (< 2 m) at any time of the day except sunrise, whereas a low abundance (≤ 1 organism) is predicted in PM regardless of depth and time-of-day. According to linear models, size was not related to depth, but was related to locality and time-of-day, with sea slugs from Arcas and Verde having similar size, and both larger than those in PM. This information suggests that this sea slug is capable of moving within the reefs and helps to understand the unique biological phenomena of kleptoplasty. [ABSTRACT FROM AUTHOR]

Abstract Background The development of nanoscale secondary ion mass spectrometry (NanoSIMS) has revolutionized the study of biological tissues by enabling, e.g., the visualization and quantification of metabolic processes at subcellular length scales. However, the associated sample preparation methods all result in some degree of tissue morphology distortion and loss of soluble compounds. To overcome these limitations an entirely cryogenic sample preparation and imaging workflow is required. Results Here, we report the development of a CryoNanoSIMS instrument that can perform isotope imaging of both positive and negative secondary ions from flat block-face surfaces of vitrified biological tissues with a mass- and image resolution comparable to that of a conventional NanoSIMS. This capability is illustrated with nitrogen isotope as well as trace element mapping of freshwater hydrozoan Green Hydra tissue following uptake of 15N-enriched ammonium. Conclusion With a cryo-workflow that includes vitrification by high pressure freezing, cryo-planing of the sample surface, and cryo-SEM imaging, the CryoNanoSIMS enables correlative ultrastructure and isotopic or elemental imaging of biological tissues in their most pristine post-mortem state. This opens new horizons in the study of fundamental processes at the tissue- and (sub)cellular level. Teaser CryoNanoSIMS: subcellular mapping of chemical and isotopic compositions of biological tissues in their most pristine post-mortem state.

Symsagittifera roscoffensis is an intertidal Acoel flatworm that forms a symbiotic relationship with the alga Tetraselmis convolutae. Members of the genus Tetraselmis are known to have a high nutritional value and have been widely used to enrich intermediate prey for fish within the aquaculture industry; therefore, S. roscoffensis could be a good candidate as a trophic shortcut to deliver algal nutrition to fish. In this study, we investigated the likelihood of five ornamental tropical freshwater and six ornamental marine fishes to consume this worm, either as live feed or in freeze-dried form. We also tested the ability of S. roscoffensis to form a symbiotic relationship with alternative algal species, analysing the nutritional profile of S. roscoffensis when grown in different media. All the experimental fish consumed live worms to some degree, with the exception of one species (Meiacanthus grammistes); the response time to the worms ranged from 1.1–68.6 s for freshwater ornamental species to 1–24 s for marine ornamental species, and in most cases, this was comparable to or shorter than their response time to the reference diet Artemia. The fishes showed no negative effects after consuming the worms. We obtained similar results with freeze-dried worms in terms of the number of worms eaten, response time, and feeding time. Symsagittifera roscoffensis was able to form a symbiotic relationship with all the tested algal species of the genus Tetraselmis, but not with members of other genera. Worms grown in nutrient media (f/2 and f/4) had significantly higher contents of protein, pigments, and total and polyunsaturated fatty acids, including eicosapentaenoic acid (20:5n − 3) and α-linolenic acid (18:3n − 3), than those grown in seawater. These results show that S. roscoffensis was acceptable to many ornamental fish species, delivering key algal ingredients that are beneficial to fish health; hence, it is a promising alternative to conventional fish feeds for the ornamental pet trade.

Acoels in the family Convolutidae are commonly found with microalgal symbionts. Convolutids can host green algal Tetraselmis and dinoflagellates within the family Symbiodiniaceae and the genus Amphidinium. The diversity of these microalgae has not been well surveyed. In this study, we used PCR and culture techniques to demonstrate the biodiversity of Tetraselmis and dinoflagellates in symbiosis with meiofaunal acoels. Here, 66 acoels were collected from seven localities around Okinawa, Ishigaki, and Kochi, Japan. While convolutids were heavily represented in this sampling, some acoels formed a clade outside Convolutidae and are potentially a new family of acoels harboring symbiotic microalgae. From the acoels collected, a total of 32 Tetraselmis and 26 Symbiodiniaceae cultures were established. Molecular phylogenies were constructed from cultured material (and from total host DNA) using the 18S rRNA gene (Tetraselmis) and 28S rRNA gene (dinoflagellates). The majority of Tetraselmis sequences grouped within the T. astigmatica clade but strains closely related to T. convolutae, T. marina, and T. gracilis were also observed. This is the first report of Tetraselmis species, other than T. convolutae, naturally associating with acoels. For dinoflagellates, members of Cladocopium and Miliolidium were observed, but most Symbiodiniaceae sequences formed clusters within Symbiodinium, grouping with S. natans, or sister to S. tridacnidorum. Several new Symbiodinium sequences from this study may represent novel species. This is the first molecular record of Miliolidium and Symbiodinium from acoels. Microalgal strains from this study will provide a necessary framework for future taxonomic studies and research on symbiotic relationships between acoels and microalgae. [ABSTRACT FROM AUTHOR]

Modern scleractinian corals can display high phenotypic plasticity, which reflects an interplay among various environmental controls, such as sediment input, water hydrodynamics or light intensity. In particular, the latter can strongly influence the morphology of coral species living across broad depth gradients. Light intensity was also a factor shaping the colonies of extinct Palaeozoic tabulate corals (Anthozoa: Tabulata). Based on gradual transitions in morphology observed in corals from the Middle Devonian (Givetian stage, ~ 385 Ma) mesophotic coral ecosystems (MCE) of the Aferdou el Mrakib reef (Anti-Atlas mountains, Morocco) and comparative material originating from different palaeobathymetric and biogeographical settings, we show that Devonian tabulate corals, such as Roseoporella and Alveolites, were characterised by high phenotypic plasticity and the ability to dramatically change their morphology depending on the inferred light conditions. Such a mechanism is similar to that observed in modern scleractinians, e.g. Porites sillimaniana. This recurring morphological theme suggests that Palaeozoic tabulate corals shared many functional characteristics of modern scleractinians. [ABSTRACT FROM AUTHOR]

Sacoglossa are known for stealing photosynthetically active chloroplasts from their macroalgal food and incorporating them into their cytosol. The nutritional support these alien organelles (kleptoplasts) provide to the slugs is still debatable. Comparing slugs starved in continuous darkness (non-photosynthetic condition) and light (photosynthetic condition) is often used to understand the contribution of the kleptoplasts to the slugs' metabolism. Here, we examined the slugs' side of starvation in darkness to better understand the effects of darkness on the slugs. We compared the gene expression profile and digestive activity of Elysia viridis, starved for one week under ambient light and continuous darkness. Starvation in darkness led to the up-regulation of genes related to glucose deficiency, while genes involved in the development, cellular organization, and reproduction were down-regulated. This specific gene expression may counteract reduced nutrient availability under non-photosynthetic conditions. Under photosynthetic conditions, kleptoplasts may have a higher nutritional value and may be able to support some metabolic processes. It appears that the slugs can only access kleptoplast photosynthates through autophagy during starvation. Nevertheless, autophagy and length reduction in darkness are highly elevated compared to light conditions, suggesting that more slug tissue is needed to satisfy the nutritional demands under non-photosynthetic conditions. Since we did not detect a gene expression related to the export of photosynthates to the slugs, our results support the hypothesis that slugs use kleptoplasts as larders accessible via autophagy. As long as the kleptoplasts are functional, they provide an energetic support, helping the slugs to reduce starvation-induced stress. [ABSTRACT FROM AUTHOR]

Background : The development of nanoscale secondary ion mass spectrometry (NanoSIMS) has revolutionized the study of biological tissues by enabling, e.g., the visualization and quantification of metabolic processes at subcellular length scales. However, the associated sample preparation methods all result in some degree of tissue morphology distortion and loss of soluble compounds. To overcome these limitations an entirely cryogenic sample preparation and imaging workflow is required. Results: Here, we report the development of a CryoNanoSIMS instrument that can perform isotope imaging of both positive and negative secondary ions from flat block-face surfaces of vitrified biological tissues with a mass- and image resolution comparable to that of a conventional NanoSIMS. This capability is illustrated with nitrogen isotope as well as trace element mapping of freshwater hydrozoan Green Hydra tissue following uptake of 15N-enriched ammonium. Conclusion: With a cryo-workflow that includes vitrification by high pressure freezing, cryo-planing of the sample surface, and cryo-SEM imaging, the CryoNanoSIMS enables correlative ultrastructure and isotopic or elemental imaging of biological tissues in their most pristine post-mortem state. This opens new horizons in the study of fundamental processes at the tissue- and (sub)cellular level. Teaser: CryoNanoSIMS: subcellular mapping of chemical and isotopic compositions of biological tissues in their most pristine post-mortem state. [ABSTRACT FROM AUTHOR]

Symsagittifera roscoffensis is an intertidal Acoel flatworm that forms a symbiotic relationship with the alga Tetraselmis convolutae. Members of the genus Tetraselmis are known to have a high nutritional value and have been widely used to enrich intermediate prey for fish within the aquaculture industry; therefore, S. roscoffensis could be a good candidate as a trophic shortcut to deliver algal nutrition to fish. In this study, we investigated the likelihood of five ornamental tropical freshwater and six ornamental marine fishes to consume this worm, either as live feed or in freeze-dried form. We also tested the ability of S. roscoffensis to form a symbiotic relationship with alternative algal species, analysing the nutritional profile of S. roscoffensis when grown in different media. All the experimental fish consumed live worms to some degree, with the exception of one species (Meiacanthus grammistes); the response time to the worms ranged from 1.1–68.6 s for freshwater ornamental species to 1–24 s for marine ornamental species, and in most cases, this was comparable to or shorter than their response time to the reference diet Artemia. The fishes showed no negative effects after consuming the worms. We obtained similar results with freeze-dried worms in terms of the number of worms eaten, response time, and feeding time. Symsagittifera roscoffensis was able to form a symbiotic relationship with all the tested algal species of the genus Tetraselmis, but not with members of other genera. Worms grown in nutrient media (f/2 and f/4) had significantly higher contents of protein, pigments, and total and polyunsaturated fatty acids, including eicosapentaenoic acid (20:5n − 3) and α-linolenic acid (18:3n − 3), than those grown in seawater. These results show that S. roscoffensis was acceptable to many ornamental fish species, delivering key algal ingredients that are beneficial to fish health; hence, it is a promising alternative to conventional fish feeds for the ornamental pet trade. [ABSTRACT FROM AUTHOR]

Planktonic foraminifera are unicellular marine zooplankton with calcite shells. Important characteristics of planktonic foraminifera include the preservability of calcite shells as microfossils in sediments and the recordability of environmental and ecological information as their shells were calcified. Some planktonic foraminifera species have been found to possess an endosymbiotic relationship with algae, known as 'photosymbiosis.' Overall, photosymbiosis is an evolutionary and nutritionally important ecology, and it also plays an important role in understanding the Earthʼs surface system in terms of material cycling and carbon cycling in particular. In this paper, I briefly review the current knowledge on planktonic foraminifera and photosymbiosis and outline the studies we have conducted so far with focus on the extraction of photosymbiotic signals and the biological phenomena concerning photosymbiosis. Finally, I discuss the prospects of further research on photosymbiotic marine protistan plankton. [ABSTRACT FROM AUTHOR]

Symsagittifera roscoffensis is a well-known member of the order Acoela that lives in symbiosis with the algae Tetraselmis convolutae during its adult stage. Its natural habitat is the eastern coast of the Atlantic, where at specific locations thousands of individuals can be found, mostly, lying in large pools on the surface of sand at low tide. As a member of the Acoela it has been thought as a proxy for ancestral bilaterian animals; however, its phylogenetic position remains still debated. In order to understand the basic structural characteristics of the acoel genome, we sequenced and assembled the genome of aposymbiotic species S. roscoffensis. The size of this genome was measured to be in the range of 910-940 Mb. Sequencing of the genome was performed using PacBio Hi-Fi technology. Hi-C and RNA-seq data were also generated to scaffold and annotate it. The resulting assembly is 1.1 Gb large (covering 118% of the estimated genome size) and highly continuous, with N50 scaffold size of 1.04 Mb. The repetitive fraction of the genome is 61%, of which 85% (half of the genome) are LTR retrotransposons. Genome-guided transcriptome assembly identified 34,493 genes, of which 29,351 are protein coding (BUSCO score 97.6%), and 30.2% of genes are spliced leader trans-spliced. The completeness of this genome suggests that it can be used extensively to characterize gene families and conduct accurate phylogenomic reconstructions. [ABSTRACT FROM AUTHOR]

Simple Summary: Climate change has made bleaching events increasingly common in coral reefs. As such, scientists are rushing to better understand what will be the outcomes of bleaching on these tropical ecosystems. However, scientific focus is mostly being given to the direct impacts promoted by these events (e.g., mass mortality of corals, coral reef decay, community transitions), with indirect ones remaining largely overlooked (e.g., impacts on trophic interactions of highly specialized animals). Organisms directly affected by bleaching display a poorer nutritional value, but the effects this may have on their predators remain largely overlooked. To address this gap in scientific research, we advocate the use of the model predator–prey pair featuring the nudibranch sea slug Berghia stephanieae and its prey, the photosymbiotic glass anemone Exaiptasia diaphana. As the two species are already used as models in other research fields, one can build upon existing knowledge to determine if and how this highly specialized sea slug, that only preys upon glass anemones, is affected in terms of survival and reproductive fitness when only bleached prey are available. Moreover, this model pair will also allow investigating if such trophic effects cascade over consecutive generations, shaping populations and ultimately ruling species survival. Bleaching events associated with climate change are increasing worldwide, being a major threat to tropical coral reefs. Nonetheless, the indirect impacts promoted by the bleaching of organisms hosting photosynthetic endosymbionts, such as those impacting trophic interactions, have received considerably less attention by the scientific community. Bleaching significantly affects the nutritional quality of bleached organisms. The consequences promoted by such shifts remain largely overlooked, namely on specialized predators that have evolved to prey upon organisms hosting photosynthetic endosymbionts and benefit nutritionally, either directly or indirectly, from the available pool of photosynthates. In the present study, we advocate the use of the model predator–prey pair featuring the stenophagous nudibranch sea slug Berghia stephanieae that preys upon the photosymbiotic glass anemone Exaiptasia diaphana to study the impacts of bleaching on trophic interactions. These model organisms are already used in other research fields, and one may benefit from knowledge available on their physiology, omics, and culture protocols under controlled laboratory conditions. Moreover, B. stephanieae can thrive on either photosymbiotic or aposymbiotic (bleached) glass anemones, which can be easily maintained over long periods in the laboratory (unlike photosymbiotic corals). As such, one can investigate if and how nutritional shifts induced by bleaching impact highly specialized predators (stenophagous species), as well as if and how such effects cascade over consecutive generations. Overall, by using this model predator–prey pair one can start to truly unravel the trophic effects of bleaching events impacting coral reef communities, as well as their prevalence over time. [ABSTRACT FROM AUTHOR]

Photosymbiosis, a mode of mixotrophy by algal endosymbiosis, provides key advantage to pelagic life in oligotrophic oceans. Despite its ecological importance, mechanisms underlying its emergence and association with the evolutionary success of photosymbiotic lineages remain unclear. We used planktonic foraminifera, a group of pelagic test-forming protists with an excellent fossil record, to reveal the history of symbiont acquisition among their three main extant clades. We used single-cell 18S rRNA gene amplicon sequencing to reveal symbiont identity and mapped the symbiosis on a phylogeny time-calibrated by fossil data. We show that the highly specific symbiotic interaction with dinoflagellates emerged in the wake of a major extinction of symbiont-bearing taxa at the end of the Eocene. In contrast, less specific and low-light adapted symbioses with pelagophytes emerged 20 million years later, in multiple independent lineages in the Late Neogene, at a time when the vertical structure of pelagic ecosystems was transformed by global cooling. We infer that in foraminifera, photosymbiosis can evolve easily and that its establishment leads to diversification and ecological dominance to such extent, that the proliferation of new symbioses is prevented by the incumbent lineages., (© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)

Abstract Background Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and species identity in shaping the associated algal community. Results We used next-generation sequencing to identify the associated algal community, and DNA barcoding to identify the diatom endosymbionts associated with species of A. lobifera, A. lessonii, and A. radiata, collected from shallow habitats (

Berghia stephanieae (Nudibranchia, Cladobranchia) is a photosymbiotic sea slug that feeds exclusively on sea anemones from the genus Exaiptasia. It then specifically incorporates dinoflagellates belonging to the Symbiodiniaceae obtained from their prey. Here, we present the complete mitochondrial genome sequence of B. stephanieae combining Oxford Nanopore long read and Illumina short-read sequencing data. The mitochondrial genome has a total length of 14,786 bp, it contains the 13 protein-encoding genes, 23 tRNAs, and two rRNAs and is similar to other nudibranchs except for the presence of a duplicated tRNA-Ser 1.

Background: The coral-Symbiodiniaceae symbiosis is fundamental for the coral reef ecosystem. Corals provide various inorganic nutrients to their algal symbionts in exchange for the photosynthates to meet their metabolic demands. When becoming symbionts, Symbiodiniaceae cells show a reduced proliferation rate and a different life history. While it is generally believed that the animal hosts play critical roles in regulating these processes, far less is known about the molecular underpinnings that allow the corals to induce the changes in their symbionts. Results: We tested symbiont cell proliferation and life stage changes in vitro in response to different nutrient-limiting conditions to determine the key nutrients and to compare the respective symbiont transcriptomic profiles to cells in hospite. We then examined the effects of nutrient repletion on symbiont proliferation in coral hosts and quantified life stage transitions in vitro using time-lapse confocal imaging. Here, we show that symbionts in hospite share gene expression and pathway activation profiles with free-living cells under nitrogen-limited conditions, strongly suggesting that symbiont proliferation in symbiosis is limited by nitrogen availability. Conclusions: We demonstrate that nitrogen limitation not only suppresses cell proliferation but also life stage transition to maintain symbionts in the immobile coccoid stage. Nutrient repletion experiments in corals further confirmed that nitrogen availability is the major factor limiting symbiont density in hospite. Our study emphasizes the importance of nitrogen in coral-algae interactions and, more importantly, sheds light on the crucial role of nitrogen in symbiont life history regulation. [ABSTRACT FROM AUTHOR]

Abstract Functional kleptoplasty is a photosymbiotic relationship, in which photosynthetically active chloroplasts serve as an intracellular symbiont for a heterotrophic host. Among Metazoa, functional kleptoplasty is only found in marine sea slugs belonging to the Sacoglossa and recently described in Rhabdocoela worms. Although functional kleptoplasty has been intensively studied in Sacoglossa, the fundamentals of the specific recognition of the chloroplasts and their subsequent incorporation are unknown. The key to ensure the initiation of any symbiosis is the ability to specifically recognize the symbiont and to differentiate a symbiont from a pathogen. For instance, in photosymbiotic cnidarians, several studies have shown that the host innate immune system, in particular scavenger receptors (SRs) and thrombospondin‐type‐1 repeat (TSR) protein superfamily, is playing a major role in the process of recognizing and differentiating symbionts from pathogens. In the present study, SRs and TSRs of three Sacoglossa sea slugs, Elysia cornigera, Elysia timida, and Elysia chlorotica, were identified by translating available transcriptomes into potential proteins and searching for receptor specific protein and/or transmembrane domains. Both receptors classes are highly diverse in the slugs, and many new domain arrangements for each receptor class were found. The analyses of the gene expression of these three species provided a set of species‐specific candidate genes, that is, SR‐Bs, SR‐Es, C‐type lectins, and TSRs, that are potentially relevant for the recognition of kleptoplasts. The results set the base for future experimental studies to understand if and how these candidate receptors are indeed involved in chloroplast recognition.

Abstract Background Photosymbiotic associations between metazoan hosts and photosynthetic dinoflagellates are crucial to the trophic and structural integrity of many marine ecosystems, including coral reefs. Although extensive efforts have been devoted to study the short-term ecological interactions between coral hosts and their symbionts, long-term evolutionary dynamics of photosymbiosis in many marine animals are not well understood. Within Bivalvia, the second largest class of mollusks, obligate photosymbiosis is found in two marine lineages: the giant clams (subfamily Tridacninae) and the heart cockles (subfamily Fraginae), both in the family Cardiidae. Morphologically, giant clams show relatively conservative shell forms whereas photosymbiotic fragines exhibit a diverse suite of anatomical adaptations including flattened shells, leafy mantle extensions, and lens-like microstructural structures. To date, the phylogenetic relationships between these two subfamilies remain poorly resolved, and it is unclear whether photosymbiosis in cardiids originated once or twice. Results In this study, we establish a backbone phylogeny for Cardiidae utilizing RNASeq-based transcriptomic data from Tridacninae, Fraginae and other cardiids. A variety of phylogenomic approaches were used to infer the relationship between the two groups. Our analyses found conflicting gene signals and potential rapid divergence among the lineages. Overall, results support a sister group relationship between Tridacninae and Fraginae, which diverged during the Cretaceous. Although a sister group relationship is recovered, ancestral state reconstruction using maximum likelihood-based methods reveals two independent origins of photosymbiosis, one at the base of Tridacninae and the other within a symbiotic Fraginae clade. Conclusions The newly revealed common ancestry between Tridacninae and Fraginae brings a possibility that certain genetic, metabolic, and/or anatomical exaptations existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats.

Photosymbiosis is one of the key features characterizing planktonic foraminifera; the number of symbiont cells within a single host has been reported to be well over thousands, meaning that photosynthesis by photosymbiosis may be a “hot spot” for primary production, especially in oligotrophic oceans. As microenvironmental conditions around foraminifera are greatly affected by rapid biological activities—such as photosynthesis and respiration—information on the photosynthetic activities of symbionts is essential to interpret the geochemical proxies recorded in foraminiferal tests (e.g., δ13C and δ18O). Recently, active chlorophyll fluorometry has been increasingly employed as a useful tool for immediate estimation of photosynthesis. However, carbon assimilation rates are the only direct indicator of the photosynthetic carbon flux. Therefore, before utilizing active fluorescence methods to understand carbon dynamics in foraminiferal symbiosis, it is necessary to confirm the relationship between the fluorescence-based photosynthetic rate [electron transport rate (ETR)] and carbon assimilation rate (P). Here, these two rates were compared for two species, Trilobatus sacculifer and Globigerinella siphonifera Type II, using 14C-tracer experiments and active fluorometric measurements by fast repetition rate fluorometry. The results showed a significant positive correlation between the P and ETR of the two species, indicating that carbon assimilation can be estimated by the fluorometric method. However, the regression slopes, which represent the apparent electron requirement for carbon assimilation (e–/C), were significantly different in the two species, and were estimated at 26.2 for T. sacculifer and 96.5 for G. siphonifera. These are strikingly high, considering the theoretically and empirically realistic e–/C values. We hypothesized that the high e–/C observed may be due in part to the use of unlabeled respiratory carbon (underestimation of P). A simple mass balance calculation suggests that a significant amount of carbon should derive from the host’s respired CO2, whose contribution is higher in G. siphonifera than in T. sacculifer. Within the context of using test geochemical parameters, such as δ13C, as paleoceanographic proxies, it is important to note that the potential magnitude of the photosynthetic effect varies among species. This attempt to couple ETR and P could comprehensively reveal an interesting perspective on the intimate interactions existing within photosymbiotic systems.

The photosymbiosis with host-specific dinoflagellates is a widespread relationship in marine organisms. Despite the evidenced biodiversity of this kind of mutualism, most research focuses on the study of scleractinian corals, and there is a lack of knowledge about other symbiotic cnidarians such as jellyfishes. The Mediterranean jellyfish Cotylorhiza tuberculata (Rhizostomae, Scyphozoa) harbors an endosymbiotic dinoflagellate of the family Symbiodiniaceae. In this study, we examine the algae distribution within the host body as well as, the pigment content and cell density of the symbiont. Furthermore, the size, morphology and fluorescence of cultured symbionts were studied under light microscopy, Imaging Flow Cytometry (IFC), and Scanning Electron Microscopy (SEM). The C:N composition and optical properties of the medusa tissue were measured to evaluate their role in the symbiosis. The medusae body was divided into two different sections to investigate the distribution of symbionts in hospite: oral arms (OA) and umbrella (UM). C:N composition of C. tuberculata was and symbiont density was significantly higher in the OA section. Mean chlorophyll a concentration of the algae was 1.33 (± 0.83) pg Chl a cell–1. The study of the pigment composition by HPLC (High Performance Liquid Chromatography), revealed the presence of 13 different pigments, being the most representative chlorophyll a, chlorophyll c2, and peridinin typical pigments of Symbiodiniaceae. Cell diameter of algae freshly isolated from the host was 8.71 ± 0.97 μm and cell growth rate was 0.52 (± 0.09) 106 cell ml–1 d–1. The presence of vegetative coccoid cells, doublet and motile mastigotes were revealed within the Symbiodiniaceae cultures. A calcifying matrix typical of Symbiodiniaceae and formed in partner with bacteria, was also observed most cultures. The umbrella tissue of the medusa absorbed at ultraviolet radiation (UVR) region, suggesting that medusae tissue protects photosymbionts from the negative effect of the high energetic UVR and attenuates the light intensity reaching algae inside the host. The presence of a dense Symbiodiniaceae population and the protection to UVR and elevated environmental irradiance provided by medusae tissue, maintain symbionts in optimal light conditions for photosynthesis and may be a reason added to explain the population success of Cotylorhiza tuberculata.

Bleaching events associated with climate change are increasing worldwide, being a major threat to tropical coral reefs. Nonetheless, the indirect impacts promoted by the bleaching of organisms hosting photosynthetic endosymbionts, such as those impacting trophic interactions, have received considerably less attention by the scientific community. Bleaching significantly affects the nutritional quality of bleached organisms. The consequences promoted by such shifts remain largely overlooked, namely on specialized predators that have evolved to prey upon organisms hosting photosynthetic endosymbionts and benefit nutritionally, either directly or indirectly, from the available pool of photosynthates. In the present study, we advocate the use of the model predator–prey pair featuring the stenophagous nudibranch sea slug Berghia stephanieae that preys upon the photosymbiotic glass anemone Exaiptasia diaphana to study the impacts of bleaching on trophic interactions. These model organisms are already used in other research fields, and one may benefit from knowledge available on their physiology, omics, and culture protocols under controlled laboratory conditions. Moreover, B. stephanieae can thrive on either photosymbiotic or aposymbiotic (bleached) glass anemones, which can be easily maintained over long periods in the laboratory (unlike photosymbiotic corals). As such, one can investigate if and how nutritional shifts induced by bleaching impact highly specialized predators (stenophagous species), as well as if and how such effects cascade over consecutive generations. Overall, by using this model predator–prey pair one can start to truly unravel the trophic effects of bleaching events impacting coral reef communities, as well as their prevalence over time.

Background: Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and species identity in shaping the associated algal community. Results: We used next-generation sequencing to identify the associated algal community, and DNA barcoding to identify the diatom endosymbionts associated with species of A. lobifera, A. lessonii, and A. radiata, collected from shallow habitats (< 15 m) in 16 sites, ranging from the Mediterranean Sea to French Polynesia. Next-generation sequencing results showed the consistent presence of Ochrophyta as the main algal phylum associated with all species and sites analysed. A significant proportion of phylotypes were classified as Chlorophyta and Myzozoa. We uncovered unprecedented diversity of algal phylotypes found in low abundance, especially of the class Bacillariophyta (i.e., diatoms). We found a significant influence of sites rather than host identity in shaping algal communities in all species. DNA barcoding revealed the consistent presence of phylotypes classified within the order Fragilariales as the diatoms associated with A. lobifera and A. lessonii, while A. radiata specimens host predominately diatoms of the order Triceratiales. Conclusions: We show that local habitat is the main factor influencing the overall composition of the algal symbiont community. However, host identity and the phylogenetic relationship among hosts is relevant in shaping the specific endosymbiont diatom community, suggesting that the relationship between diatom endosymbiont and hosts plays a crucial role in the evolutionary history of the genus Amphistegina. The capacity of Amphistegina species to associate with a diverse array of diatoms, and possibly other algal groups, likely underpins the ecological success of these crucial calcifying organisms across their extensive geographic range. [ABSTRACT FROM AUTHOR]

Berghia stephanieae (Nudibranchia, Cladobranchia) is a photosymbiotic sea slug that feeds exclusively on sea anemones from the genus Exaiptasia. It then specifically incorporates dinoflagellates belonging to the Symbiodiniaceae obtained from their prey. Here, we present the complete mitochondrial genome sequence of B. stephanieae combining Oxford Nanopore long read and Illumina short-read sequencing data. The mitochondrial genome has a total length of 14,786 bp, it contains the 13 protein-encoding genes, 23 tRNAs, and two rRNAs and is similar to other nudibranchs except for the presence of a duplicated tRNA-Ser 1. [ABSTRACT FROM AUTHOR]

Photosymbiosis indicates a long-term association between animals and photosynthetic organisms. It has been mainly investigated in photosymbiotic cnidarians, while other photosymbiotic associations have been largely neglected. The acoel Symsagittifera roscoffensis lives in obligatory symbiosis with the microalgal Tetraselmis convolutae and has recently emerged as alternative model to study photosymbiosis. Here, we investigated the effects of Bisphenol A, a common plastic additive, on two pivotal stages of its lifecycle: aposymbiotic juvenile development and photosymbiogenesis. Based on our results, this pollutant altered the development of the worms and their capacity to engulf algae from the environment at concentrations higher than the levels detected in seawater, yet aligning with those documented in sediments of populated areas. Data provide novel information about the effects of pollutants on photosymbiotic associations and prompt the necessity to monitor their concentrations in marine environmental matrices. • Photosymbiosis is an association between animals and photosynthetic organisms. • Symsagittifera roscoffensis is an acoel worm that lives in symbiosis with a green alga. • Bisphenol A, a common pollutant, impairs the development of aposymbiotic juveniles. • Bisphenol A prevents S. roscoffensis to acquire the symbiont from the environment. • Pollutants are potentially harmful for photosymbiotic associations. [ABSTRACT FROM AUTHOR]

The unique symbiosis between a vertebrate salamander, Ambystoma maculatum, and unicellular green alga, Oophila amblystomatis, involves multiple modes of interaction. These include an ectosymbiotic interaction where the alga colonizes the egg capsule, and an intracellular interaction where the alga enters tissues and cells of the salamander. One common interaction in mutualist photosymbioses is the transfer of photosynthate from the algal symbiont to the host animal. In the A. maculatum–O. amblystomatis interaction, there is conflicting evidence regarding whether the algae in the egg capsule transfer chemical energy captured during photosynthesis to the developing salamander embryo. In experiments where we took care to separate the carbon fixation contributions of the salamander embryo and algal symbionts, we show that inorganic carbon fixed by A. maculatum embryos reaches 2% of the inorganic carbon fixed by O. amblystomatis algae within an egg capsule after 2 h in the light. After 2 h in the dark, inorganic carbon fixed by A. maculatum embryos is 800% of the carbon fixed by O. amblystomatis algae within an egg capsule. Using photosynthesis inhibitors, we show that A. maculatum embryos and O. amblystomatis algae compete for available inorganic carbon within the egg capsule environment. Our results confirm earlier studies suggesting a role of heterotrophic carbon fixation during vertebrate embryonic development. Our results also show that the considerable capacity of developing A. maculatum embryos for inorganic carbon fixation precludes our ability to distinguish any minor role of photosynthetically transferred carbon from algal symbionts to host salamanders using bicarbonate introduced to the egg system as a marker.

Abstract The Gulf of Aqaba is home to three giant clam species with differing ecological niches and levels of photosymbiotic activity. Giant clams grow a two‐layered shell where the outer layer is precipitated in close association with photosymbiont‐bearing siphonal mantle, and the inner layer is grown in association with the light‐starved inner mantle. We collected 39 shells of the three species (the cosmopolitan Tridacna maxima and T. squamosa, as well as the rare endemic T. squamosina) and measured carbon and oxygen isotope ratios from inner and outer shell layers, to test for differences among species and between the layers of their shells. T. squamosina records higher temperatures of shell formation as determined by oxygen isotope paleothermometry, consistent with its status as an obligately shallow‐dwelling species. However, the known negative fractionation imparted on tissue carbon isotopes by photosymbiotic algae did not produce measurable offsets in the carbonate δ13C values of the more symbiotic T. squamosina and T. maxima compared to the more heterotrophic T. squamosa. Across all species, outer shell layers recorded mean growth temperatures 1.8°C higher than corresponding inner layers, which we propose is a function of the high insolation, low albedo microenvironment of the outer mantle, and potentially the activity of the symbionts themselves. Population‐wide isotopic sampling of reef‐dwelling bivalve shells can help constrain the ecological niches of rare taxa and help reconstruct their internal physiology.

Coral reefs' high productivity has been attributed mainly to photosymbioses between the coral animal and algae of the family Symbiodiniaceae, with recognition that the host can increase algal photosynthesis by concentrating nutrients and enhancing the efficiency of light absorption. Here, we propose that an additional effect, consumption of carbohydrate by the host, may also enhance algal photosynthesis. We examine evidence from symbiosis between terrestrial plants and root fungi that indicates a link between carbohydrate consumption by the symbiotic partner and photosynthetic upregulation in the plant system. In addition, we review evidence from free‐living algae manipulated to exude carbohydrate into the external medium, which was associated with strong upregulation of photosynthetic capacity. We offer suggestions on how host‐induced carbohydrate release may increase photosynthesis rates in the symbionts in the intact photosymbiosis and how this relationship evolved. [ABSTRACT FROM AUTHOR]

Functional kleptoplasty is a photosymbiotic relationship, in which photosynthetically active chloroplasts serve as an intracellular symbiont for a heterotrophic host. Among Metazoa, functional kleptoplasty is only found in marine sea slugs belonging to the Sacoglossa and recently described in Rhabdocoela worms. Although functional kleptoplasty has been intensively studied in Sacoglossa, the fundamentals of the specific recognition of the chloroplasts and their subsequent incorporation are unknown. The key to ensure the initiation of any symbiosis is the ability to specifically recognize the symbiont and to differentiate a symbiont from a pathogen. For instance, in photosymbiotic cnidarians, several studies have shown that the host innate immune system, in particular scavenger receptors (SRs) and thrombospondin‐type‐1 repeat (TSR) protein superfamily, is playing a major role in the process of recognizing and differentiating symbionts from pathogens. In the present study, SRs and TSRs of three Sacoglossa sea slugs, Elysia cornigera, Elysia timida, and Elysia chlorotica, were identified by translating available transcriptomes into potential proteins and searching for receptor specific protein and/or transmembrane domains. Both receptors classes are highly diverse in the slugs, and many new domain arrangements for each receptor class were found. The analyses of the gene expression of these three species provided a set of species‐specific candidate genes, that is, SR‐Bs, SR‐Es, C‐type lectins, and TSRs, that are potentially relevant for the recognition of kleptoplasts. The results set the base for future experimental studies to understand if and how these candidate receptors are indeed involved in chloroplast recognition. [ABSTRACT FROM AUTHOR]

The deep‐sea sedimentary record of Ocean Drilling Program Site 690 (Weddell Sea) has figured prominently in the study of an ancient (~56 Ma) global warming event referred to as the Paleocene‐Eocene Thermal Maximum (PETM). Yet discrepancies in the timing, amplitude, and structure of the isotopic excursions marking the PETM exist between the bulk‐carbonate and planktic foraminifer stable isotope (δ13C and δ18O) records of this reference section. A recent study invoked size‐dependent sediment mixing (SDSM) to reconcile the discrepancies between these parallel δ13C records. Here we report supplementary stable isotope data compiled from size‐segregated planktic foraminifer shells that further elucidate the effects of SDSM on the Site 690 PETM section. Our records reveal a stratigraphic sequence where the carbon (CIE) and oxygen (OIE) isotope excursions marking the onset of PETM conditions are first registered by larger shells, confirming that smaller‐sized pre‐CIE shells have been more intensely mixed and preferentially displaced up‐section into the overlying CIE interval. The size‐dependent manner in which the CIE and OIE are recorded by asymbiotic subbotinids indicates that the transitory loss of size‐dependent δ13C signatures in photosymbiotic taxa (acarininids) at Site 690 is an artifact of SDSM. Synthetic bulk‐carbonate δ13C records generated with two end‐member (pre‐CIE versus CIE materials) sediment‐mixing curves readily reproduce the series of "steps" seen in published bulk‐carbonate δ13C records of the CIE, suggesting that these fine‐scale features may also be artifacts of SDSM and varying rates of carbonate sedimentation. Key Points: Size‐dependent sediment mixing accounts for multiple vagaries in stable isotope records of the iconic PETM section from ODP Site 690The Site 690 bulk‐carbonate record has been smoothed and distorted by preferential reworking of fine‐fraction carbonateTemporary loss of the δ13C‐size signature of photosymbiosis is an artifact of size‐dependent sediment mixing, not a paleoecological signal [ABSTRACT FROM AUTHOR]

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The Gulf of Aqaba is home to three giant clam species with differing ecological niches and levels of photosymbiotic activity. Giant clams grow a two‐layered shell where the outer layer is precipitated in close association with photosymbiont‐bearing siphonal mantle, and the inner layer is grown in association with the light‐starved inner mantle. We collected 39 shells of the three species (the cosmopolitan Tridacna maxima and T. squamosa, as well as the rare endemic T. squamosina) and measured carbon and oxygen isotope ratios from inner and outer shell layers, to test for differences among species and between the layers of their shells. T. squamosina records higher temperatures of shell formation as determined by oxygen isotope paleothermometry, consistent with its status as an obligately shallow‐dwelling species. However, the known negative fractionation imparted on tissue carbon isotopes by photosymbiotic algae did not produce measurable offsets in the carbonate δ13C values of the more symbiotic T. squamosina and T. maxima compared to the more heterotrophic T. squamosa. Across all species, outer shell layers recorded mean growth temperatures 1.8°C higher than corresponding inner layers, which we propose is a function of the high insolation, low albedo microenvironment of the outer mantle, and potentially the activity of the symbionts themselves. Population‐wide isotopic sampling of reef‐dwelling bivalve shells can help constrain the ecological niches of rare taxa and help reconstruct their internal physiology. Plain Language Summary: Giant clams are large bivalves which live on reefs and, like corals, also contain algae living as symbionts within their tissue. These clams record temperature via the ratio of two isotopes of oxygen (the heavier 18O and lighter 16O) in their shell, and it has been proposed that their carbon isotope ratios are influenced by their symbionts. The three species of giant clam from around the Gulf of Aqaba (Northern Red Sea): Tridacna squamosina, T. squamosa, and T. maxima, are thought to live in different habitats and to have different amounts of photosynthesis. To test this, we collected several dozen shells to compare the oxygen and carbon isotopes of each species. We found that the rare T. squamosina records the highest average growth temperatures, which supports previous observations that it lives only in shallow water. Giant clams also have two layers in their shells, and we compared the isotopes of the layers. We found that the Sun‐drenched outer shell layer records higher temperatures than the inner one, which we propose is due to solar heating of the algae‐filled outermost tissue. Symbiosis does not appear to change the carbon isotope ratios between the layers or between species with different amounts of photosynthesis. More work is needed to investigate how ecology and physiology influence the isotopes between bivalve species and within their shells. Key Points: The outer shell layer of Tridacna is depleted in 18O compared to the inner layer, corresponding to a 1.7°C higher reconstructed temperatureThere is no significant difference in δ13C value between species, but δ18O is lower in the obligately shallow‐dwelling Tridacna squamosinaWhile carbon isotopes did not track different degrees of photosymbiosis, oxygen isotopes can be used to constrain ecological niche partitioning for rare species [ABSTRACT FROM AUTHOR]

Background: Photosymbiotic associations between metazoan hosts and photosynthetic dinoflagellates are crucial to the trophic and structural integrity of many marine ecosystems, including coral reefs. Although extensive efforts have been devoted to study the short-term ecological interactions between coral hosts and their symbionts, long-term evolutionary dynamics of photosymbiosis in many marine animals are not well understood. Within Bivalvia, the second largest class of mollusks, obligate photosymbiosis is found in two marine lineages: the giant clams (subfamily Tridacninae) and the heart cockles (subfamily Fraginae), both in the family Cardiidae. Morphologically, giant clams show relatively conservative shell forms whereas photosymbiotic fragines exhibit a diverse suite of anatomical adaptations including flattened shells, leafy mantle extensions, and lens-like microstructural structures. To date, the phylogenetic relationships between these two subfamilies remain poorly resolved, and it is unclear whether photosymbiosis in cardiids originated once or twice. Results: In this study, we establish a backbone phylogeny for Cardiidae utilizing RNASeq-based transcriptomic data from Tridacninae, Fraginae and other cardiids. A variety of phylogenomic approaches were used to infer the relationship between the two groups. Our analyses found conflicting gene signals and potential rapid divergence among the lineages. Overall, results support a sister group relationship between Tridacninae and Fraginae, which diverged during the Cretaceous. Although a sister group relationship is recovered, ancestral state reconstruction using maximum likelihood-based methods reveals two independent origins of photosymbiosis, one at the base of Tridacninae and the other within a symbiotic Fraginae clade. Conclusions: The newly revealed common ancestry between Tridacninae and Fraginae brings a possibility that certain genetic, metabolic, and/or anatomical exaptations existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats. [ABSTRACT FROM AUTHOR]

Radiolarians are a group of ubiquitous, yet poorly understood, large protists that often harbor photosymbionts. We studied the solitary radiolarian Thalassicolla nucleata by analyzing the transcriptome of its holobiont. We found that T. nucleata contained two dinoflagellate symbionts, one photosymbiont Brandtodinium sp., and one putative Peridiniales parasite. Through comparisons of gene expressions of Brandtodinium sp. and those of a close relative from a free-living culture, we found that the Brandtodinium sp. maintained its photosynthetic activities, but altered its carbon metabolism dramatically in hospite. Gene expression data also suggested carbon and nitrogen exchange between the host and photosymbiont and that lectin-glycan interaction might play an important role in host-symbiont recognition.

Cyanobacteria are common in symbiotic relationships with diverse multicellular organisms (animals, plants, fungi) in terrestrial environments and with single-celled heterotrophic, mixotrophic, and autotrophic protists in aquatic environments. In the sunlit zones of aquatic environments, diverse cyanobacterial symbioses exist with autotrophic taxa in phytoplankton, including dinoflagellates, diatoms, and haptophytes (prymnesiophytes). Phototrophic unicellular cyanobacteria related to Synechococcus and Prochlorococcus are associated with a number of groups. N2-fixing cyanobacteria are symbiotic with diatoms and haptophytes. Extensive genome reduction is involved in the N2-fixing endosymbionts, most dramatically in the unicellular cyanobacteria associated with haptophytes, which have lost most of the photosynthetic apparatus, the ability to fix C, and the tricarboxylic acid cycle. The mechanisms involved in N2-fixing symbioses may involve more interactions beyond simple exchange of fixed C for N. N2-fixing cyanobacterial symbioses are widespread in the oceans, even more widely distributed than the best-known free-living N2-fixing cyanobacteria, suggesting they may be equally or more important in the global ocean biogeochemical cycle of N.Despite their ubiquitous nature and significance in biogeochemical cycles, cyanobacterium-phytoplankton symbioses remain understudied and poorly understood. [ABSTRACT FROM AUTHOR]