Some species of planktic foraminifera inhabiting oligotrophic surface water environments are in an obligate symbiotic relationship with dinoflagellate microalgae, which can assimilate carbon (C) through photosynthesis. However, the mechanism and dynamics of C photosynthate translocation to the foraminiferal host, and related benefits for the dinoflagellates in this symbiotic association, are poorly constrained. As a consequence, the role of planktic foraminifera as autotroph organisms in ocean surface ecosystems is not well understood. Here, we performed pulse-chase experiments with 13C-enriched dissolved inorganic carbon, followed by TEM and quantitative NanoSIMS isotopic imaging to visualize photosynthetic C assimilation by individual symbiotic dinoflagellates and subsequent translocation to their Orbulina universa host. Although most of the dinoflagellate population migrates out of the host endoplasm onto external spines during the day, our observations show that a small fraction remains inside the host cell during daytime. All symbionts, whether outside or inside the foraminifera cell, effectively assimilate C into starch nodules during daytime photosynthesis. At the onset of night, all dinoflagellates from the exterior spine–ectoplasm region migrate back into the foraminiferal cell. During the night, respiration by dinoflagellates and carbon translocation to the host, likely in the form of lipids, greatly reduces the abundance of starch in dinoflagellates. Dinoflagellate mitosis is only observed at night, with a substantial contribution of carbon fixed during the previous day contributing to the production of new biomass.

The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets its nitrogen (N) requirements by preying on zooplankton, and that its symbiotic dinoflagellates recycle metabolic 'waste ammonium' for their N pool. However, these conclusions were derived from bulk ¹⁵N-enrichment experiments and model calculations, and our understanding of N assimilation and exchange between the foraminifer host cell and its symbiotic dinoflagellates remains poorly constrained. Here, we present data from pulse-chase experiments with ¹³C-enriched inorganic carbon, ¹⁵N-nitrate, and ¹⁵N-ammonium, as well as a ¹³C- and ¹⁵N- enriched heterotrophic food source, followed by TEM (transmission electron microscopy) coupled to NanoSIMS (nanoscale secondary ion mass spectrometry) isotopic imaging to visualize and quantify C and N assimilation and translocation in the symbiotic system. High levels of ¹⁵N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with ¹⁵N-ammonium, indicating efficient ammonium assimilation. Only weak ¹⁵N-assimilation was observed after incubation with ¹⁵N-nitrate. Feeding foraminifers with ¹³C- and ¹⁵N-labelled food resulted in dinoflagellates that were labelled with ¹⁵N, thereby confirming the transfer of ¹⁵N-compounds from the digestive vacuoles of the foraminifer to the symbiotic dinoflagellates, likely through recycling of ammonium. These observations are important for N isotope-based palaeoceanographic reconstructions, as they show that δ¹⁵N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates.

Endosymbioses have shaped the evolutionary trajectory of life and remain ecologically important. Investigating oceanic photosymbioses can illuminate how algal endosymbionts are energetically exploited by their heterotrophic hosts and inform on putative initial steps of plastid acquisition in eukaryotes. By combining three-dimensional subcellular imaging with photophysiology, carbon flux imaging, and transcriptomics, we show that cell division of endosymbionts (Phaeocystis) is blocked within hosts (Acantharia) and that their cellular architecture and bioenergetic machinery are radically altered. Transcriptional evidence indicates that a nutrient-independent mechanism prevents symbiont cell division and decouples nuclear and plastid division. As endosymbiont plastids proliferate, the volume of the photosynthetic machinery volume increases 100-fold in correlation with the expansion of a reticular mitochondrial network in close proximity to plastids. Photosynthetic efficiency tends to increase with cell size, and photon propagation modeling indicates that the networked mitochondrial architecture enhances light capture. This is accompanied by 150-fold higher carbon uptake and up-regulation of genes involved in photosynthesis and carbon fixation, which, in conjunction with a ca.15-fold size increase of pyrenoids demonstrates enhanced primary production in symbiosis. Mass spectrometry imaging revealed major carbon allocation to plastids and transfer to the host cell. As in most photosymbioses, microalgae are contained within a host phagosome (symbiosome), but here, the phagosome invaginates into enlarged microalgal cells, perhaps to optimize metabolic exchange. This observation adds evidence that the algal metamorphosis is irreversible. Hosts, therefore, trigger and benefit from major bioenergetic remodeling of symbiotic microalgae with potential consequences for the oceanic carbon cycle. Unlike other photosymbioses, this interaction represents a so-called cytoklepty, which is a putative initial step toward plastid acquisition.