Advertisement

Photosymbiosis in Marine Planktonic Protists

  • Johan Decelle
  • Sébastien Colin
  • Rachel A. Foster

Abstract

Some of the most enigmatic components in the plankton are the diverse eukaryotic protists that live in close association with one or more partners. Mutualistic and commensal planktonic interactions are most commonly encountered in the oligotrophic open ocean at tropical and subtropical latitudes. They are functionally and ecologically distinct, and involve a great taxonomic diversity of single-celled partners. Protists like Foraminifera, Radiolaria, dinoflagellates and diatoms can all harbor microalgal symbionts of eukaryotic and prokaryotic origin inside (endosymbiosis) and/or outside (ectosymbiosis) their cytoplasm. Such symbioses (photosymbioses) combine phototrophy, heterotrophy and sometimes di-nitrogen (N2) fixation (reduction of N2 to ammonium). Symbiotic microorganisms therefore represent an important component of marine ecosystems and play a role in the food web and biogeochemical cycling (e.g., carbon and nitrogen). Despite their important ecological function and early recognition in the late nineteenth century, our knowledge about the diversity, distribution, and metabolic exchanges for many of the photosymbioses remains rudimentary compared with the other marine and terrestrial symbioses. Recent technical advances in single-cell genomics and imaging have greatly improved our understanding about planktonic symbioses. This review aims to present and compare many eukaryote–eukaryote and eukaryote–prokaryote photosymbioses described so far in the open ocean with an emphasis on their ecology and potential function in the ecosystem.

Keywords

Symbiosis Plankton Protists Open ocean Mutualism Single-cell Cyanobiont N2 fixation 

Notes

Acknowledgments

JD and SC are supported by the project OCEANOMICS, which has received funding from the French Government, managed by the Agence Nationale de la Recherche, under the grant agreement “Investissement d’Avenir” ANR-11-BTBR-0008. RAF’s contribution is funded by the Knut and Alice Wallenberg Foundation (Sweden) and the National Science Foundation (USA). We thank the coordinators and members of the Tara-Oceans expedition. We are grateful to Christian Sardet, John Dolan, Katsunori Kimoto and Ken Furuya for providing pictures of symbiotic organisms.

References

  1. Alldredge AL, Jones BM (1973) Hastigerina pelagica: Foraminiferal habitat for planktonic dinoflagellates. Mar Biol 22:131–135CrossRefGoogle Scholar
  2. Anderson OR (1983) Radiolaria. Springer, New YorkCrossRefGoogle Scholar
  3. Anderson OR (2012) Living together in the plankton: a survey of marine protist symbioses. Acta Protozool 52:1–10Google Scholar
  4. Anderson OR, Matsuoka A (1992) Endocytoplasmic microalgae and bacteroids within the central capsule of the Radiolarian Dictycoryne truncatum. Symbiosis 12:237–247Google Scholar
  5. Anderson OR, Swanberg NR, Bennett P (1983a) Fine structure of yellow-brown symbionts (Prymnesiida) in solitary Radiolaria and their comparison with similar acantharian symbionts. J Protozool 30:718–722CrossRefGoogle Scholar
  6. Anderson OR, Swanberg NR, Bennett P (1983b) Assimilation of symbiont-derived photosynthates in some solitary and colonial Radiolaria. Mar Biol 77:265–269CrossRefGoogle Scholar
  7. Annenkova NV, Lavrov DV, Belikov SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:22–236CrossRefGoogle Scholar
  8. Aurahs R, Göker M, Grimm GW et al (2009) Using the multiple analysis approach to reconstruct phylogenetic relationships among planktonic Foraminifera from highly divergent and length-polymorphic SSU rDNA sequences. Bioinform Biol Insights 3:155–177PubMedCentralPubMedGoogle Scholar
  9. Balech E (1962) Tintinnoinea y dinoflagellata del Pacifico. Rev Mus Argent Cienc Nat “Bernardino Rivadavia” Cienc Zool 8:1–249Google Scholar
  10. 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 70:73–86CrossRefGoogle Scholar
  11. Bijma J, Erez J, Hemleben C (1990) Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers. J Foraminifer Res 20:117–127CrossRefGoogle Scholar
  12. Brandt K (1881) Über das Zusammenleben von Algen und Tieren. Biol Zentbl 1:524–527Google Scholar
  13. Buck KR, Bentham WN (1998) A novel symbiosis between a cyanobacterium, Synechococcus sp., an aplastidic protist, Solenicola setigera, and a diatom, Leptocylindrus mediterraneus, in the open ocean. Mar Biol 132:349–355CrossRefGoogle Scholar
  14. Cachon M, Caram B (1979) A symbiotic green alga, Pedinomonas symbiotica sp. nov. (Prasinophyceae), in the radiolarian Thalassolampe margarodes. Phycologia 18:177–184CrossRefGoogle Scholar
  15. Caron DA, Swanberg NR (1990) The ecology of planktonic sarcodines. Rev Aquat Sci 3:147–180Google Scholar
  16. Caron DA, Michaels AF, Swanberg NR et al (1995) Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J Plankton Res 17:103–129CrossRefGoogle Scholar
  17. Carpenter EJ, Foster RA (2002) Marine cyanobacterial symbioses. In: Rai A, Bergman B, Rasmussan U (eds) Cyanobacteria in symbiosis. Kluwer Publishers, Dordrecht, pp 11–17Google Scholar
  18. Carpenter EJ, Janson S (2000) Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). J Phycol 36:540–544CrossRefGoogle Scholar
  19. Casey R, Partridge TM, Sloan JR (1971) Radiolarian life spans, mortality rates, and seasonality gained from recent sediment and plankton samples. In: Farinacci A (ed) Proceedings of the 2nd Planktonic conference, Roma 1970, vol 1. Tecnoscienza, Roma, pp 159–165Google Scholar
  20. Chesnick JM, Cox ER (1987) Synchronized sexuality of an algal symbiont and its dinoflagellate host, Peridinium balticum (Levander) Lemmermann. Biosystems 21:69–78PubMedCrossRefGoogle Scholar
  21. Daugbjerg N, Jensen MH, Hansen PJ (2013) Using nuclear-encoded LSU and SSU rDNA sequences to identify the eukaryotic endosymbiont in Amphisolenia bidentata (Dinophyceae). Protist 164:411–422PubMedCrossRefGoogle Scholar
  22. de Bary AH (1878) Ueber Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp 121–126Google Scholar
  23. Decelle J (2013) New perspectives on the functioning and evolution of photosymbiosis in plankton: mutualism or parasitism? Commun Integr Biol 6(4):e24560PubMedCentralPubMedCrossRefGoogle Scholar
  24. Decelle J, Probert I, Bittner L et al (2012a) An original mode of symbiosis in open ocean plankton. Proc Natl Acad Sci U S A 109:18000–18005PubMedCentralPubMedCrossRefGoogle Scholar
  25. Decelle J, Siano R, Probert I et al (2012b) Multiple microalgal partners in symbiosis with the acantharian Acanthochiasma sp. (Radiolaria). Symbiosis 58:233–244CrossRefGoogle Scholar
  26. Decelle J, Suzuki N, Mahé F et al (2012c) Molecular phylogeny and morphological evolution of the Acantharia (Radiolaria). Protist 163:435–450PubMedCrossRefGoogle Scholar
  27. Dufrêne YF (2002) Atomic force microscopy, a powerful tool in microbiology. J Bacteriol 184:5205–5213PubMedCentralPubMedCrossRefGoogle Scholar
  28. Elbrächter M, Qi YZ (1998) Aspects of Noctiluca (Dinophyceae) population dynamics. In: Anderson DM, Cambella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, London, pp 315–335Google Scholar
  29. Erickson JS, Hashemi N, Sullivan JM et al (2012) In situ phytoplankton analysis: there’s plenty of room at the bottom. Anal Chem 84:839–850PubMedCrossRefGoogle Scholar
  30. Escalera L, Reguera B, Takishita K et al (2011) Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae). Protist 162:304–311PubMedCrossRefGoogle Scholar
  31. Faber WW, Anderson OR, Lindsey JL et al (1988) Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis: I. occurrence and stability of two mutually exclusive chrysophyte endosymbionts and their ultrastructure. J Foraminifer Res 18:334–343CrossRefGoogle Scholar
  32. Fairbanks RG, Wiebe PH (1980) Foraminifera and chlorophyll maximum: vertical distribution, seasonal succession, and paleoceanographic significance. Science 209:1524–1526PubMedCrossRefGoogle Scholar
  33. Farnelid H, Tarangkoon W, Hansen G et al (2010) Putative N2-fixing heterotrophic bacteria associated with dinoflagellate-cyanobacteria consortia in the low nitrogen Indian Ocean. Aquat Microb Ecol 61:105–117CrossRefGoogle Scholar
  34. Febvre J, Febvre-Chevalier C (1979) Ultrastructural study of zooxanthellae of three species of Acantharia (protozoa: actinopoda) with details of their taxonomic position in the Prymnesiales (Prymnesiophyceae, Hibberd, 1976). J Mar Biol Assoc UK 59:215–226CrossRefGoogle Scholar
  35. Figueroa RI, Bravo I, Fraga S et al (2009) The life history and cell cycle of Kryptoperidinium foliaceum, a dinoflagellate with two eukaryotic nuclei. Protist 160:285–300PubMedCrossRefGoogle Scholar
  36. Foissner W, Berger H, Schaumburg J (1999) Identification and ecology of limnetic plankton ciliates. Bavarian State Office for Water Management, MunichGoogle Scholar
  37. Foster R, O’Mullan GD (2008) Chapter 27—nitrogen fixing and nitrifying symbioses in the marine environment. In: Capone DG, Bronk DA, Mulholland MR et al (eds) Nitrogen in the marine environment, 2nd edn. Elsevier Inc., Amsterdam, pp 1197–1218CrossRefGoogle Scholar
  38. Foster RA, Zehr JP (2006) Characterization of diatom-cyanobacteria symbioses on the basis of nifH, hetR, and 16S rRNA sequences. Environ Microbiol 8:1913–1925PubMedCrossRefGoogle Scholar
  39. Foster R, Carpenter EJ, Bergman B (2006a) Unicellular cyanobionts in open ocean dinoflagellates, radiolarians, and tintinnids: ultrastructural characterization and immuno-localization of phycoerythrin and nitrogenase. J Phycol 42:453–463CrossRefGoogle Scholar
  40. Foster RA, Collier JL, Carpenter EJ (2006b) Reverse transcription PCR amplification of cyanobacterial symbiont 16S rRNA sequences from single non-photosynthetic eukaryotic marine planktonic host cells. J Phycol 42:243–250CrossRefGoogle Scholar
  41. Foster RA, Goebel NL, Zehr JP (2010) Isolation of Calothrix rhizosoleniae (cyanobacteria) strain SC01 from Chaetoceros (Bacillariophyta) spp. diatoms of the Subtropical North Pacific Ocean. J Phycol 46:1028–1037CrossRefGoogle Scholar
  42. Foster RA, Kupyers MMM, Vagner T et al (2011) Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5:1484–1493PubMedCentralPubMedCrossRefGoogle Scholar
  43. Frada M, Young M, Cachão M et al (2010) A guide to extant coccolithophores (Calcihaptophycidae, Haptophyta) using light microscopy. J Nannoplankton Res 31:58–112Google Scholar
  44. Frank AB (1877) Über die biologischen Verhältnisse des Thallus einiger Krusten-Flechten. Beitr Biol Pflanz 2:132–200Google Scholar
  45. Fujiki T, Takagi H, Kimoto K, Kurasawa A, Yuasa T, Mino Y (2014) Assessment of algal photosynthesis in planktic foraminifers by fast repetition rate fluorometry. J Plankton Res 36:1403–1407CrossRefGoogle Scholar
  46. Fukuda Y, Endoh H (2006) New details from the complete life cycle of the red-tide dinoflagellate Noctiluca scintillans (Ehrenberg) McCartney. Eur J Protistol 42:209–219PubMedCrossRefGoogle Scholar
  47. Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from Foraminifera and Radiolaria. Mol Biol Evol 13:1192–1197PubMedCrossRefGoogle Scholar
  48. Gast RJ, Caron DA (2001) Photosymbiotic associations in planktonic Foraminifera and Radiolaria. Hydrobiologia 461:1–7CrossRefGoogle Scholar
  49. Gast RJ, McDonnell TA, Caron DA (2000) srDNA-based taxonomic affinities of algal symbionts from a planktonic foraminifer and a solitary radiolarian. J Phycol 36:172–177CrossRefGoogle Scholar
  50. Gast RJ, Moran DM, Dennett MR et al (2007) Kleptoplastidy in an Antarctic dinoflagellate: caught in evolutionary transition? Environ Microbiol 9:39–45PubMedCrossRefGoogle Scholar
  51. Gast RJ, Sanders RW, Caron DA (2009) Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol 17:563–569PubMedCrossRefGoogle Scholar
  52. Geddes P (1878) Sur la fonction de la chlorophylle avec les planaires vertes. CR Séances Acad Sci Paris 87:1095–1097Google Scholar
  53. Gómez F (2007) The consortium of the Protozoan Solenicola setigera and the diatom Leptocylindrus mediterraneus in the Pacific Ocean. Acta Protozool 46:15–24Google Scholar
  54. Gómez F, Moreira D, López-García P (2010) Molecular phylogeny of the dinoflagellates Podolampas and Blepharocysta (Peridiniales, Dinophyceae). Phycologia 49:212–220CrossRefGoogle Scholar
  55. Gómez F, López-García P, Moreira D (2011) Molecular phylogeny of dinophysoid dinoflagellates: the systematic position of Oxyphysis oxytoxoides and the Dinophysis hastata group (Dinophysales, Dinophyceae). J Phycol 47:393–406CrossRefGoogle Scholar
  56. Haeckel E (1887) Report on the Radiolaria collected by H.M.S. Challenger during the years 1873–1876. Rep Sci Res Voyage HMS Challenger, Zool 18:1–1803Google Scholar
  57. Hagino K, Onuma R, Kawachi M et al (2013) Discovery of an endosymbiotic nitrogen-fixing cyanobacterium UCYN-A in Braarudosphaera bigelowii (Prymnesiophyceae). PLoS One 8:e81749PubMedCentralPubMedCrossRefGoogle Scholar
  58. Hansen PJ (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J Eukaryot Microbiol 58:203–214PubMedCrossRefGoogle Scholar
  59. Hansen PJ, Fenchel T (2006) The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar Biol Res 2:169–177CrossRefGoogle Scholar
  60. Hansen PJ, Miranda L, Azanza R (2004) Green Noctiluca scintillans: a dinoflagellate with its own greenhouse. Mar Ecol Prog Ser 275:79–87CrossRefGoogle Scholar
  61. Harrison PJ, Furuya K, Glibert PM et al (2011) Geographical distribution of red and green Noctiluca scintillans. Chin J Oceanol Limnol 29:807–831CrossRefGoogle Scholar
  62. Hasle GR (1975) Some living marine species of the diatom family Rhizosoleniaceae. Nova Hedwig Beih 53:99–140Google Scholar
  63. Hemleben C, Spindler M (1983) Recent advances in research on living planktonic Foraminifera. Utrecht Micropalaeontol Bull 30:141–170Google Scholar
  64. Hemleben C, Spindler M, Anderson OR (1989) Modern planktonic Foraminifera. Springer, HeidelbergCrossRefGoogle Scholar
  65. Henjes J, Assmy P, Klaas C et al (2007) Response of the larger protozooplankton to an iron-induced phytoplankton bloom in the Polar Frontal Zone of the Southern Ocean (EisenEx). Deep Sea Res I 54(5):774–791CrossRefGoogle Scholar
  66. Hilton JA, Foster RA, Tripp HJ et al (2013) Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat Commun 4:1767PubMedCentralPubMedCrossRefGoogle Scholar
  67. Hirose E, Hirabayashi S, Hori K et al (2006) UV protection in the photosymbiotic ascidian Didemnum molle inhabiting different depths. Zool Sci 23:57–63PubMedCrossRefGoogle Scholar
  68. Huber BT, Bijma J, Spero HJ (1996) Blue-water SCUBA collection of planktonic Foraminifera. In: Lang MA, Baldwin CC (eds) Methods and techniques of underwater research. Proceedings of the American Academy of Underwater Sciences. Smithsonian Institution, Washington, DC, pp 127–132Google Scholar
  69. Huxley TH (1851) Upon Thalassicolla, a new zoophyte. Ann Mag Nat Hist Ser 2 8:433–442Google Scholar
  70. Imanian B, Keeling PJ (2007) The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages. BMC Evol Biol 7:172PubMedCentralPubMedCrossRefGoogle Scholar
  71. Imanian B, Pombert JF, Keeling PJ (2010) The complete plastid genomes of the two ‘dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum. PloS One 5:e10711PubMedCentralPubMedCrossRefGoogle Scholar
  72. Jakobsen HH, Hansen PJ, Larsen J (2000) Growth and grazing responses of two chloroplast-retaining dinoflagellates: effect of irradiance and prey species. Mar Ecol Prog Ser 201:121–128CrossRefGoogle Scholar
  73. Janson S, Carpenter EJ, Bergman B (1995) Immunolabeling of phycoerythrin, ribulose 1, 5-biphosphate carboxylase/oxygenase and nitrogenase in the unicellular cyanobionts of Ornithocercus spp. (Dinophyceae). Phycologia 34:171–176CrossRefGoogle Scholar
  74. Janson S, Wouters J, Bergman B et al (1999) Host specificity in the Richelia-diatom symbiosis revealed by hetR gene sequence analysis. Environ Microbiol 1:431–438PubMedCrossRefGoogle Scholar
  75. Johnson MD (2011) Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J Eukaryot Microbiol 58:185–195PubMedCrossRefGoogle Scholar
  76. Jørgensen BB, Erez J, Revsbech NP et al (1985) Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes. Limnol Oceanogr 30:1253–1267CrossRefGoogle Scholar
  77. Kodama Y, Fujishima M (2010) Secondary symbiosis between Paramecium and Chlorella cells. In: Jeon KW (ed) International review of cell and molecular biology, vol 279. Elsevier Inc., Amsterdam, pp 33–77Google Scholar
  78. Krupke A, Musat N, LaRoche J et al (2013) In situ detection and N2 and C fixation rates of uncultivated cyanobacteria groups: UCYN-A and UCYN-B. Syst Appl Microbiol 36:259–271PubMedCrossRefGoogle Scholar
  79. Lampitt RS, Salter I, John D (2009) Radiolaria: major exporters of organic carbon to the deep ocean. Global Biogeochem Cycles 23:GB1010CrossRefGoogle Scholar
  80. Lee JJ (2006) Algal symbiosis in larger Foraminifera. Symbiosis 42:63–75Google Scholar
  81. Lobban CS, Schefter M, Simpson AGB et al (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar Biol 141:207–208CrossRefGoogle Scholar
  82. Lombard F, Labeyrie L, Michel E et al (2009) Modelling the temperature dependent growth rates of planktic Foraminifera. Mar Micropaleontol 70:1–7CrossRefGoogle Scholar
  83. Lucas IAN (1991) Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia 33:213–224CrossRefGoogle Scholar
  84. Madhu NV, Jyothibabu R, Maheswaran PA et al (2012) Enhanced chlorophyll a and primary production in the northern Arabian Sea during the spring intermonsoon due to green Noctiluca scintillans bloom. Mar Biol Res 8:182–188CrossRefGoogle Scholar
  85. Malfatti F, Azam F (2009) Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat Microb Ecol 58:1–14CrossRefGoogle Scholar
  86. Malkassian A, Nerini D, van Dijk MA et al (2011) Functional analysis and classification of phytoplankton based on data from an automated flow cytometer. Cytometry A 79A:263–275CrossRefGoogle Scholar
  87. Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New HavenGoogle Scholar
  88. Massera Bottazzi E, Andreoli MG (1981) “Blooming” of Acantharia (Protozoa-Sarcodina) in the southern Atlantic Ocean. Quad Lab Technol 3:637Google Scholar
  89. Mayali X, Weber PK, Brodie EL et al (2012) High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use. ISME J 6:1210–1221PubMedCentralPubMedCrossRefGoogle Scholar
  90. Michaels AF (1988) Vertical distribution and abundance of Acantharia and their symbionts. Mar Biol 97:559–569CrossRefGoogle Scholar
  91. Michaels AF (1991) Acantharian abundance and symbiont productivity at the VERTEX seasonal station. J Plankton Res 13:399–418CrossRefGoogle Scholar
  92. Michaels AF, Caron DA, Swanberg NR et al (1995) Planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda – abundance, biomass and vertical flux. J Plankton Res 17:131–163CrossRefGoogle Scholar
  93. Moisander PH, Beinhart RA, Hewson I et al (2010) Unicellular cyanobacterial distributions broaden oceanic N2 fixation domain. Science 327:1512–1514PubMedCrossRefGoogle Scholar
  94. Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518PubMedCrossRefGoogle Scholar
  95. Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104:8627–8633PubMedCentralPubMedCrossRefGoogle Scholar
  96. Moya A, Tambutte S, Tambutte E et al (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata: implications for “light-enhanced calcification”. J Exp Biol 209:3413–3419PubMedCrossRefGoogle Scholar
  97. Müller J (1858) Über die Thalassicollen, Polycystinen und Acanthometren des Mittelmeeres. Abh Königl Preuß AkadWiss, Berlin, pp 1–62Google Scholar
  98. Murray J (1897) On the distribution of the pelagic Foraminifera at the surface and on the floor of the ocean. Nat Sci (Ecol) 11:17–27Google Scholar
  99. Musat N, Halm H, Winterholler B et al (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci U S A 105:17861–17866PubMedCentralPubMedCrossRefGoogle Scholar
  100. Musat N, Foster RA, Vagner T et al (2011) Detecting metabolic activities in single cells with emphasis on nanoSIMS. FEMS Microbiol Rev 36:486–511PubMedCrossRefGoogle Scholar
  101. Okaichi T, Ochi T, Tada K et al (1991) Isolation and culture of Pedinomonas noctilucae, a symbiont of Noctiluca scintillans of Gulf of Thailand. In: Proceedings of the second IOC/WESTPAC symposium, Penang, pp 166–176Google Scholar
  102. Olson RJ, Sosik HM (2007) A submersible imaging-in-flow instrument to analyze nano- and microplankton: imaging FlowCytobot. Limnol Oceanogr Methods 5:195–203CrossRefGoogle Scholar
  103. Padmakumar KB, Cicily L, Shaji A et al (2012) Symbiosis between the stramenopile protist Solenicola setigera and the diatom Leptocylindrus mediterraneus in the north eastern Arabian Sea. Symbiosis 56:97–101CrossRefGoogle Scholar
  104. Parke M, Manton I (1967) Specific identity of algal symbiont in Convoluta roscoffensis. J Mar Biol Assoc UK 47:445–457CrossRefGoogle Scholar
  105. Pedrós-Alió C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4:449–466PubMedCrossRefGoogle Scholar
  106. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid Foraminifera in Hawaii. Mol Phylogenet Evol 56:492–497PubMedCrossRefGoogle Scholar
  107. Probert I, Siano R, Poirier C et al (2014) Brandtodinium gen. nov. and B. nutricula comb. nov. (Dinophyceae), a dinoflagellate commonly found in symbiosis with polycystine radiolarians. J Phycol 50:388–399CrossRefGoogle Scholar
  108. Rampi L (1952) Ricerche sul Microplancton di superficie del Pacifico tropicale. Bull Inst Océanogr (Monaco) 1014:1–16Google Scholar
  109. Rink S, Kühl M, Bijma J et al (1998) Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa. Mar Biol 131:583–595CrossRefGoogle Scholar
  110. Rodenacker K, Hense B, Jütting U et al (2006) Automatic analysis of aqueous specimens for phytoplankton structure recognition and population estimation. Microsc Res Tech 69:708–720PubMedCrossRefGoogle Scholar
  111. Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202–209PubMedCrossRefGoogle Scholar
  112. Schewiakoff WT (1926) The Acantharia. Fauna e Flora del Golfo di Napoli 37:1–755Google Scholar
  113. Schoemann V, Becquevort S, Stefels J et al (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53:43–66CrossRefGoogle Scholar
  114. Schulze K, Tillich UM, Dandekar T et al (2013) PlanktoVision – an automated analysis system for the identification of phytoplankton. BMC Bioinformatics 14:115PubMedCentralPubMedCrossRefGoogle Scholar
  115. Schütt F (1895) Die Peridineen der Plankton-Expedition. Ergeb Plankton-Exped Humboldt-Stifung 4:1–170Google Scholar
  116. Schweikert M, Elbrächter M (2004) First ultrastructural investigations of the consortium between a phototrophic eukaryotic endocytobiont and Podolampas bipes (Dinophyceae). Phycologia 43:614–623CrossRefGoogle Scholar
  117. Schwendener S (1868) Untersuchungen über den Flechtenthallus. Beitr Wiss Bot 6:195–207Google Scholar
  118. Shaked Y, de Vargas C (2006) Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts. Mar Ecol Prog Ser 325:59–71CrossRefGoogle Scholar
  119. Sheik AR, Brussaard CPD, Lavik G et al (2012) Viral infection of Phaeocystis globosa impedes release of chitinous star-like structures: quantification using single cell approaches. Environ Microbiol 15:1441–1451PubMedCrossRefGoogle Scholar
  120. Siano R, Montresor M, Probert I et al (2010) Pelagodinium gen. nov and P. béii comb. nov., a dinoflagellate symbiont of planktonic Foraminifera. Protist 161:385–399PubMedCrossRefGoogle Scholar
  121. Sournia A (1986) Atlas du phytoplancton marin. I. Cyanophycees, Dictyophycees, Dinophycees et Raphidophycees, vol 1. CNRS, Paris, pp 1–219Google Scholar
  122. 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
  123. Spero HJ, Angel DL (1991) Planktonic sarcodines: microhabitat for oceanic dinoflagellates. J Phycol 27:187–195CrossRefGoogle Scholar
  124. Spindler M, Hemleben C, Bayer U et al (1979) Lunar periodicity of reproduction in the planktonic foraminifer Hastigerina pelagica. Mar Ecol Prog Ser 1:61–64CrossRefGoogle Scholar
  125. Stoecker DK, Silver MW, Michaels AE (1988–1989) Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Mar Microb Food Webs 3:79–100Google Scholar
  126. Stoecker DK, Gustafson DE, Verity PG (1996) Micro- and mesoprotozooplankton at 140°W in the equatorial Pacific: heterotrophs and mixotrophs. Aquat Microb Ecol 10:273–282CrossRefGoogle Scholar
  127. Stoecker DK, Johnson MD, de Vargas C et al (2009) Acquired phototrophy in aquatic protists. Aquat Microb Ecol 57:279–310CrossRefGoogle Scholar
  128. Sunda W, Kieber DJ, Kiene RP et al (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320PubMedCrossRefGoogle Scholar
  129. Suzuki N, Ogane K, Aita Y et al (2009) Distribution patterns of the radiolarian nuclei and symbionts using DAPI-fluorescence. Bull Natl Mus Nat Sci Ser B 35:169–182Google Scholar
  130. Swanberg NR, Caron DA (1991) Patterns of sarcodine feeding in epipelagic oceanic plankton. J Plankton Res 13:287–322CrossRefGoogle Scholar
  131. Sweeney BM (1976) Pedinomonas noctilucae (Prasinophyceae), the flagellate symbiotic in Noctiluca (Dinophyceae) in Southeast Asia. J Phycol 12:460–464Google Scholar
  132. Sweeney BM (1978) Ultrastructure of Noctiluca miliaris (Pyrrophyta) with green flagellate symbionts. J Phycol 14:116–120CrossRefGoogle Scholar
  133. Takahashi O, Mayama S, Matsuoka A (2003) Host-symbiont associations of polycystine Radiolaria: epifluorescence microscopic observation of living Radiolaria. Mar Micropaleontol 49:187–194CrossRefGoogle Scholar
  134. Tang YZ, Dobbs FC (2007) Green autofluorescence in dinoflagellates, diatoms, and other microalgae and its implications for vital staining and morphological studies. Appl Environ Microbiol 73:2306–2313PubMedCentralPubMedCrossRefGoogle Scholar
  135. Tarangkoon W, Hansen G, Hansen P (2010) Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes. Aquat Microb Ecol 58:197–213CrossRefGoogle Scholar
  136. Taylor FJR (1982) Symbioses in marine microplankton. Ann Inst Oceanogr Paris (Nova Ser) 58:61–90Google Scholar
  137. Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118PubMedCrossRefGoogle Scholar
  138. Thompson A, Foster RA, Krupke A et al (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546PubMedCrossRefGoogle Scholar
  139. Tizard TH, Mosely HN, Buchanan JY et al (1885) Narrative of the cruise of H.M.S. “Challenger”, with a general account of the scientific results of the expedition. Sci Rep Voyage HMS Challenger 1873–1876, Narrative 1:511–1110Google Scholar
  140. Tripp HJ, Bench SR, Turk KA et al (2010) Metabolic streamlining in an open ocean nitrogen-fixing cyanobacterium. Nature 464:90–94PubMedCrossRefGoogle Scholar
  141. Van Bergeijk SA, Stal LJ (2001) Dimethylsulfoniopropionate and dimethylsulfide in the marine flatworm Convoluta roscoffensis and its algal symbiont. Mar Biol 138:209–216CrossRefGoogle Scholar
  142. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 30:277–293CrossRefGoogle Scholar
  143. Villareal TA (1989) Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocaceae) symbiosis. Br Phycol J 24:357–365CrossRefGoogle Scholar
  144. Villareal TA (1990) Laboratory culture and preliminary characterization of the nitrogen-fixing Rhizosolenia-Richelia symbiosis. Mar Ecol 11:117–132CrossRefGoogle Scholar
  145. Webster NS, Taylor MW, Behnam F et al (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082PubMedCentralPubMedGoogle Scholar
  146. Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694PubMedCrossRefGoogle Scholar
  147. Yost DM, Mitchelmore CL (2009) Dimethylsulfoniopropionate (DMSP) lyase activity in different strains of the symbiotic alga Symbiodinium microadriaticum. Mar Ecol Prog Ser 386:61–70CrossRefGoogle Scholar
  148. Yuasa T, Takahashi O (2014) Ultrastructural morphology of the reproductive swarmers of Sphaerozoum punctatum (Huxley) from the East China Sea. Eur J Protistol 50:194–204PubMedCrossRefGoogle Scholar
  149. Yuasa T, Horiguchi T, Mayama S et al (2012) Ultrastructural and molecular characterization of symbionts in Dictyocoryne profunda (polycystine radiolarian). Symbiosis 57:51–55CrossRefGoogle Scholar
  150. Zeder M, Ellrott A, Amann R (2011) Automated sample area definition for high-throughput microscopy. Cytometry A 79A:306–310CrossRefGoogle Scholar
  151. Zehr JP, Waterbury JB, Turner PJ et al (2001) Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412:635–638PubMedCrossRefGoogle Scholar
  152. Zehr JP, Bench SR, Carter BJ et al (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322:1110–1112PubMedCrossRefGoogle Scholar
  153. Zetsche EM, Meysman FJR (2012) Dead or alive? Viability assessment of micro- and mesoplankton. J Plankton Res 34:493–509CrossRefGoogle Scholar
  154. Zwirglmaier K, Jardillier L, Ostrowski M et al (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10:147–161PubMedGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  • Johan Decelle
    • 1
  • Sébastien Colin
    • 2
  • Rachel A. Foster
    • 3
  1. 1.Sorbonne UniversitésRoscoffFrance
  2. 2.CNRS, UMR 7144RoscoffFrance
  3. 3.Department of Ecology, Environment and Plant SciencesStockholm UniversityStockholmSweden

Personalised recommendations