Marine Biology

, 165:104 | Cite as

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

  • Charlotte LeKieffreEmail author
  • Howard J. Spero
  • Ann D. Russell
  • Jennifer S. Fehrenbacher
  • Emmanuelle Geslin
  • Anders Meibom
Original paper


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.



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.

Supplementary material

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Supplementary material 1 (PDF 532 kb)
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Supplementary material 2 (PDF 244 kb)
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Supplementary material 3 (PDF 201 kb)
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Supplementary material 4 (PDF 267 kb)
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Supplementary material 5 (PDF 417 kb)


  1. Anderson OR, Bé AWH (1976) The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates. J Foraminifer Res 6:1–21. CrossRefGoogle Scholar
  2. Anderson OR, Lee JJ (1991) Cytology and fine structure. In: Lee JJ (eds) Biology of foraminifera. Academic Press, London, pp 7–40Google Scholar
  3. Anderson OR, Swanberg NR, Bennett P (1983) Assimilation of symbiont-derived photosynthates in some solitary and colonial radiolaria. Mar Biol 77:265–269CrossRefGoogle Scholar
  4. Bé AWH, Hutson WH (1977) Ecology of planktonic foraminifera and biogeographic patterns of life and fossil assemblages in the Indian Ocean. Micropaleontology 23:369. CrossRefGoogle Scholar
  5. Bé AWH, Hemleben C, Anderson OR, Spindler M, Hacunda J, Tuntivate-Choy S, Be AWH (1977) Laboratory and field observations of living planktonic foraminifera. Micropaleontology 23:155–179. CrossRefGoogle Scholar
  6. Bé AWH, Spero HJ, Anderson OR (1982) Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer. Mar Biol 70:73–86. CrossRefGoogle Scholar
  7. Caromel AGM, Schmidt DN, Phillips JC, Rayfield EJ (2014) Hydrodynamic constraints on the evolution and ecology of planktic foraminifera. Mar Micropaleontol 106:69–78. CrossRefGoogle Scholar
  8. Caron DA, Bé AW, Anderson OR (1981) Effects of variations in light intensity on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture. J Mar Biol Assoc UK 62:435–451CrossRefGoogle Scholar
  9. Caron DA, Michaels AF, Swanberg NR, Howse FA (1995) Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J Plankton Res 17:103–129CrossRefGoogle Scholar
  10. Ceh J, Kilburn MR, Cliff JB, Raina J-B, van Keulen M, Bourne DG (2013) Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol 3:2393–2400. CrossRefGoogle Scholar
  11. Clode PL, Stern RA, Marshall AT (2007) Subcellular imaging of isotopically labeled carbon compounds in a biological sample by ion microprobe (NanoSIMS). Microsc Res Tech 70:220–229. CrossRefPubMedGoogle Scholar
  12. Dodge JD, Crawford RM (1971) A fine-structural survey of dinoflagellate pyrenoids and food-reserves. Bot J Linn Soc 64:105–115CrossRefGoogle Scholar
  13. Doyle RW, Poore RV (1974) Nutrient competition and division synchrony in phytoplankton. J Exp Mar Biol Ecol 14:201–210. CrossRefGoogle Scholar
  14. Duguay LE, Taylor DL (1978) Primary production and calcification by the soritid foraminifer Archais angulatus (Fichtel & Moll). J Eukaryot Microbiol 25:356–361Google Scholar
  15. Faber WW, Anderson OR, Lindsey JL, Caron DA (1988) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralia; I, Occurrence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. J Foraminifer Res 18:334–343. CrossRefGoogle Scholar
  16. Hansen HJ (1975) On feeding and supposed buoyancy mechanism in four recent globigerinid foraminifera from the Gulf of Elat, Israel. Rev Esp Micropaleontol 7:325–337Google Scholar
  17. Hemleben C, Spindler M, Breitinger I, Deuser WG (1985) Field and laboratory studies on the ontogeny and ecology of some globorotaliid species from the Sargasso Sea off Bermuda. J Foraminifer Res 15:254–272. CrossRefGoogle Scholar
  18. Hemleben C, Spindler M, Anderson OR (1989) Modern planktonic foraminifera. Springer, New YorkCrossRefGoogle Scholar
  19. Hofmann DK, Kremer BP (1981) Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): significance of endosymbiotic dinoflagellates. Mar Biol 65:25–33. CrossRefGoogle Scholar
  20. Hoppe P, Cohen S, Meibom A (2013) NanoSIMS: technical aspects and applications in cosmochemistry and biological geochemistry. Geostand Geoanal Res 37:111–154. CrossRefGoogle Scholar
  21. Hottinger L, Dreher D (1974) Differentiation of protoplasm in Nummulitidae (foraminifera) from Elat, Red Sea. Mar Biol 25:41–61CrossRefGoogle Scholar
  22. Jørgensen BB, Erez J, Revsbech P, Cohen Y (1985) Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes1: symbiotic photosynthesis. Limnol Oceanogr 30:1253–1267. CrossRefGoogle Scholar
  23. Kellogg RB, Patton JS (1983) Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp. Mar Biol 75:137–149. CrossRefGoogle Scholar
  24. Köhler-Rink S, Kühl M (2005) The chemical microenvironment of the symbiotic planktonic foraminifer Orbulina universa. Mar Biol Res 1:68–78. CrossRefGoogle Scholar
  25. Kopp C, Pernice M, Domart-Coulon I, Djediat C, Spangenberg JE, Alexander DTL, Hignette M, Meziane T, Meibom A (2013) Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. mBio 4:e00052-13. PubMedPubMedCentralCrossRefGoogle Scholar
  26. Kopp C, Wisztorski M, Revel J, Mehiri M, Dani V, Capron L, Carette D, Fournier I, Massi L, Mouajjah D, Pagnotta S, Priouzeau F, Salzet M, Meibom A, Sabourault C (2015a) MALDI-MS and NanoSIMS imaging techniques to study cnidarian–dinoflagellate symbioses. Zoology 118:125–131. CrossRefPubMedGoogle Scholar
  27. Kopp C, Domart-Coulon I, Escrig S, Humbel BM, Hignette M, Meibom A (2015b) Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. mBio 6:e02299-14. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Krupke A, Mohr W, LaRoche J, Fuchs BM, Amann RI, Kuypers MM (2015) The effect of nutrients on carbon and nitrogen fixation by the UCYN-A–haptophyte symbiosis. ISME J 9:1635–1647. CrossRefPubMedGoogle Scholar
  29. Lee JJ (1983) Perspective on algal endosymbionts in larger foraminifera. Int Rev Cytol 14:49–77Google Scholar
  30. Lee JJ, Zucker W (1969) Algal flagellate symbiosis in the foraminifer Archaias. J Protozoology 16:71–81. CrossRefGoogle Scholar
  31. Lee JJ, Freudenthal HD, Kossoy V, Bé A (1965) Cytological observations on two planktonic Foraminifera, Globigerina bulloides d’Orbigny, 1826, and Globigerinoides ruber (d’Orbigny, 1839) Cushman, 1927*†‡. J Eukaryot Microbiol 12:531–542Google Scholar
  32. LeKieffre C, Spangenberg JE, Mabilleau G, Escrig S, Meibom A, Geslin E (2017) Surviving anoxia in marine sediments: the metabolic response of ubiquitous benthic foraminifera (Ammonia tepida). PLoS ONE 12:e0177604. CrossRefPubMedPubMedCentralGoogle Scholar
  33. LeKieffre C, Bernhard JM, Mabilleau G, Filipsson HL, Meibom A, Geslin E (2018) An overview of cellular ultrastructure in benthic foraminifera: New observations of rotalid species in the context of existing literature. Mar Micropaleontol 138:12–32. CrossRefGoogle Scholar
  34. Leutenegger S (1977) Ultrastructure de foraminifères perforés et imperforés ainsi que de leurs symbiontes. Cah Micropaléontologie 3:1–52Google Scholar
  35. Leutenegger S (1984) Symbiosis in benthic foraminifera; specificity and host adaptations. J Foraminifer Res 14:16–35CrossRefGoogle Scholar
  36. Musat N, Stryhanyuk H, Bombach P, Adrian L, Audinot J-N, Richnow HH (2014) The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS. Syst Appl Microbiol 37:267–276. CrossRefPubMedGoogle Scholar
  37. Muscatine L, Karakashian SJ, Karakashian MW (1967) Soluble extracellular products of algae symbiotic with a ciliate, a sponge and a mutant hydra. Comp Biochem Physiol 20:1–12. CrossRefGoogle Scholar
  38. Nomaki H, Bernhard JM, Ishida A, Tsuchiya M, Uematsu K, Tame A, Kitahashi T, Takahata N, Sano Y, Toyofuku T (2016) Intracellular isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments: results of nitrate and sulfate labeling experiments. Front Microbiol 7:163. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nomaki H, LeKieffre C, Escrig S, Meibom A, Yagyu S, Richardson EA, Matsuzaki T, Murayama M, Geslin E, Bernhard JM (2018) Innovative TEM-coupled approaches to study foraminiferal cells. Mar Micropaleontol 138:90–104. CrossRefGoogle Scholar
  40. Nuñez J, Renslow R, Cliff JB, Anderton CR (2018) NanoSIMS for biological applications: current practices and analyses. Biointerphases 13:03B301. CrossRefGoogle Scholar
  41. Patton JS, Burris JE (1983) Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar Biol 75:131–136. CrossRefGoogle Scholar
  42. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S (2012) A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis. ISME J 6:1314–1324CrossRefPubMedPubMedCentralGoogle Scholar
  43. Pernice M, Dunn SR, Tonk L, Dove S, Domart-Coulon I, Hoppe P, Schintlmeister A, Wagner M, Meibom A (2015) A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals. Environ Microbiol 17:3570–3580. CrossRefPubMedGoogle Scholar
  44. Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM (2012) Look@NanoSIMS—a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol 14:1009–1023. CrossRefPubMedGoogle Scholar
  45. Preiss J (1982) Regulation of the biosynthesis and degradation of starch. Annu Rev Plant Physiol 33:431–454CrossRefGoogle Scholar
  46. Rhumbler L (1911) Die Foraminiferen (Thalamophoren) der Plankton-Expedition, Teil 1: Die allgemeinen Organisationsverhaltnisse der ForaminiferenGoogle Scholar
  47. Rink S, Kühl M, Bijma J, Spero HJ (1998) Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa. Mar Biol 131:583–595CrossRefGoogle Scholar
  48. Röttger R, Berger WH (1972) Benthic foraminifera: morphology and growth in clone cultures of Heterostegina depressa. Mar Biol 15:89–94CrossRefGoogle Scholar
  49. RStudio Team (2016) RStudio: Integrated Development for R. RStudio Inc., BostonGoogle Scholar
  50. Schlichter D, Svoboda A, Kremer BP (1983) Functional autotrophy of Heteroxenia fuscescens (Anthozoa: Alcyonaria): carbon assimilation and translocation of photosynthates from symbionts to host. Mar Biol 78:29–38. CrossRefGoogle Scholar
  51. Schmitz K, Kremer BP (1977) Carbon fixation and analysis of assimilates in a coral-dinoflagellate symbiosis. Mar Biol 42:305–313. CrossRefGoogle Scholar
  52. Smith AM, Denyer K, Martin C (1997) The synthesis of the starch granule. Annu Rev Plant Biol 48:67–87CrossRefGoogle Scholar
  53. Spero HJ (1987) Symbiosis in the planktonic foraminifer, Orbulina universa, and the isolation of its symbiotic dinoflagellate, Gymnodinium béii sp. nov. J Phycol 23:307–317CrossRefGoogle Scholar
  54. Spero HJ (1988) Ultrastructural examination of chamber morphogenesis and biomineralization in the planktonic foraminifer Orbulina universa. Mar Biol 99:9–20. CrossRefGoogle Scholar
  55. Spero HJ, Parker SL (1985) Photosynthesis in the symbiotic planktonic foraminifer Orbulina universa, and its potential contribution to oceanic primary productivity. J Foraminifer Res 15:273–281CrossRefGoogle Scholar
  56. Taylor DL (1968) In situ studies on the cytochemistry and ultrastructure of a symbiotic marine dinoflagellate. J Mar Biol Assoc UK 48:349–366. CrossRefGoogle Scholar
  57. Trench RK (1971) The physiology and biochemistry of Zooxanthellae symbiotic with marine coelenterates. II. Liberation of fixed 14C by Zooxanthellae in vitro. Proc R Soc Lond B Biol Sci 177:237–250CrossRefGoogle Scholar
  58. Trench RK (1979) The cell biology of plant-animal symbiosis. Annu Rev Plant Physiol 30:485–531CrossRefGoogle Scholar
  59. Uhle ME, Spero HJ, Lea DW, Ruddiman WF, Engel MH (1999) The fate of nitrogen in the Orbulina universa foraminifera–symbiont system determined by nitrogen isotope analyses of shell-bound organic matter. Limnol Ocean 44:1968–1977CrossRefGoogle Scholar
  60. Whitehead LF (2003) Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J Exp Biol 206:3149–3157. CrossRefPubMedGoogle Scholar
  61. Wilkerson FP, Muller G, Muscatine PL (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014CrossRefGoogle Scholar
  62. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694. CrossRefPubMedGoogle Scholar
  63. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC)Ecole Polytechnique Fédérale de Lausanne (EPFL)LausanneSwitzerland
  2. 2.UMR CNRS 6112-LPG-BIAF, Université d’AngersAngers CedexFrance
  3. 3.Department of Earth and Planetary SciencesUniversity of California DavisDavisUSA
  4. 4.College of Earth, Ocean, and Atmospheric SciencesOregon State UniversityCorvallisUSA
  5. 5.Center for Advanced Surface Analysis, Institute of Earth SciencesUniversity of LausanneLausanneSwitzerland

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