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Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host


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.

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We gratefully acknowledge the staff of the University of Southern California, Wrigley Marine Science Center for field and laboratory assistance. We thank Team Catalina 2014 (Tom Bergamaschi, Elisa Bonnin, Oscar Branson, Edward Chu, Kate Holland, Elliot Schoenig, and Jordan Snyder) for their skilled participation. The electron microscopy platform at the University of Lausanne (Switzerland) is thanked for expert advice and access to equipment. This collaboration was established by a chance meeting between the authors during a research visit to the Alfred Wegener Institute, Bremerhaven Germany, as part of a Humboldt Research award to HJS. We thank the Alexander von Humboldt Foundation for helping create this opportunity through its support. The work was supported by the Swiss National Science Foundation (Grant no. 200021_149333) and the US National Science Foundation (OCE-1261516). The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.

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Correspondence to Charlotte LeKieffre.

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LeKieffre, C., Spero, H.J., Russell, A.D. et al. Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host. Mar Biol 165, 104 (2018).

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