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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.

Photosymbiosis is widespread and ecologically important in the oceanic plankton but remains poorly studied. Here, we used multimodal subcellular imaging to investigate the photosymbiosis between colonial Collodaria and their microalga dinoflagellate (Brandtodinium). We showed that this symbiosis is very dynamic whereby symbionts interact with different host cells via extracellular vesicles within the colony. 3D electron microscopy revealed that the photosynthetic apparatus of the microalgae was more voluminous in symbiosis compared to free-living while the mitochondria volume was similar. Stable isotope probing coupled with NanoSIMS showed that carbon and nitrogen were stored in the symbiotic microalga in starch granules and purine crystals, respectively. Nitrogen was also allocated to the algal nucleolus. In the host, low 13C transfer was detected in the Golgi. Metal mapping revealed that intracellular iron concentration was similar in free-living and symbiotic microalgae (ca 40 ppm) and two-fold higher in the host, whereas copper concentration increased in symbionts and was detected in the host cell and extracellular vesicles. Sulfur concentration was around two times higher in symbionts (chromatin and pyrenoid) than their host. This study improves our understanding on the functioning of this oceanic photosymbiosis and paves the way for more studies to further assess its biogeochemical significance.

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. N-2-fixing cyanobacteria are symbiotic with diatoms and haptophytes. Extensive genome reduction is involved in the N-2-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 N-2-fixing symbioses may involve more interactions beyond simple exchange of fixed C for N. N-2-fixing cyanobacterial symbioses are widespread in the oceans, even more widely distributed than the best-known free-living N-2-fixing cyanobacteria, suggesting they may be equally or more important in the global ocean biogeochemical cycle of N.

This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research

Differential carbon and oxygen stable isotope (delta C-13 and delta O-18) fractionation between planktonic foraminifera test calcite and sea water related to ecology and life stage confound the potential for reconstructing palaeo-water column temperature and carbon gradients. Multi-species analysis and strict selection of test sizes are useful methods for identifying these fractionation processes, also known as 'vital effects', in fossil taxa. However, there are a limited number of species with adequate size-controlled data sets, needed for ground truthing the approach in the modern. Here we report delta C-13 and delta O-18 measurements made on twelve species of modern planktonic foraminifera across a range of fourteen tightly constrained size windows from a tropical Indian Ocean core top sample. This data set includes more test size windows per species, especially from the smallest (identifiable) test size-classes, and a wider range of species than previously attempted. We use the size controlled delta O-18 calcite trajectories to infer depth habitats and calculate species-specific calcification temperatures. The temperatures are then used to constrain species-specific calcification depths along the modern vertical temperature profile in the western tropical Indian Ocean. By overlaying the per species delta C-13 calcite trajectories on local water column delta C-13(DIC) profiles, we estimate if and when (i.e. at which test sizes) the planktonic foraminifera species investigated approach ambient delta C-13(DIC) values. The profiling shows significant size-controlled delta C-13 deviation from seawater values in all species at some life/growth stage, which we attribute to (i) metabolic fractionation in tests <150-300 mu m (juveniles of all species and small adults), and; (ii) photosymbiont fractionation, affecting large tests (>similar to 300 mu m) of mixed layer photosymbiotic taxa. For most species there is a size-window where these effects appear to be at a m, AuthorCount:5

Acantharia (Radiolaria) are widespread and abundant heterotrophic marine protists, some of which can host endosymbiotic eukaryotic microalgae. Although this photosymbiotic association was first described at the end of the 19th century, the diversity of the symbiotic microalgae remains poorly characterized. Here, we examined the identity of the microalgae associated with the acantharian species Acanthochiasma sp. by sequencing partial 18S and internal transcribed spacer (ITS) ribosomal DNA genes from cultured symbionts and directly from isolated holobiont specimens. Single Acanthochiasma cells contained multiple symbiotic partners, including distantly related dinoflagellates (Heterocapsa sp., Pelagodinium sp., Azadinium sp. and Scrippsiella sp.) as well as a haptophyte (Chrysochromulina sp.). This original association of multiple symbiotic microalgae within a single host cell raises questions about the specificity and functioning of the relationship. These microalgae exhibit the common ecological feature of being abundant and widely distributed in coastal and oceanic waters, some occasionally forming extensive blooms. Some of the microalgal genera found in association with Acanthochiasma (i.e. Pelagodinium and Chrysochromulina) are known to occur in symbiosis with other heterotrophic protists such as Foraminifera and other Radiolaria, whereas Heterocapsa, Scrippsiella and Azadinium have never previously been reported to be involved in putative symbiotic relationships. The unusual association unveiled in this study contributes to our understanding of the ecological and evolutionary significance of photosymbiosis in Acantharia and also provides new insights into the nature of such partnerships in the planktonic realm.

Fromont, J., Huggett, M.J., Lengger, S.K., Grice, K., Schönberg, C.H.L. (2015). Characterization of Leucetta prolifera, a calcarean cyanosponge from south-western Australia, and its symbionts in Journal of the Marine Biological Association of the United Kingdom, 96(Special issue 2), 541-552. Available here.