Skip to main content

Photosymbiosis in Marine Planktonic Protists

  • Chapter

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.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Alldredge AL, Jones BM (1973) Hastigerina pelagica: Foraminiferal habitat for planktonic dinoflagellates. Mar Biol 22:131–135

    Article  Google Scholar 

  • Anderson OR (1983) Radiolaria. Springer, New York

    Book  Google Scholar 

  • Anderson OR (2012) Living together in the plankton: a survey of marine protist symbioses. Acta Protozool 52:1–10

    Google Scholar 

  • Anderson OR, Matsuoka A (1992) Endocytoplasmic microalgae and bacteroids within the central capsule of the Radiolarian Dictycoryne truncatum. Symbiosis 12:237–247

    Google Scholar 

  • 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 30:718–722

    Article  Google Scholar 

  • Anderson OR, Swanberg NR, Bennett P (1983b) Assimilation of symbiont-derived photosynthates in some solitary and colonial Radiolaria. Mar Biol 77:265–269

    Article  CAS  Google Scholar 

  • Annenkova NV, Lavrov DV, Belikov SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:22–236

    Article  Google Scholar 

  • 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 3:155–177

    PubMed Central  CAS  PubMed  Google Scholar 

  • Balech E (1962) Tintinnoinea y dinoflagellata del Pacifico. Rev Mus Argent Cienc Nat “Bernardino Rivadavia” Cienc Zool 8:1–249

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Bijma J, Erez J, Hemleben C (1990) Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers. J Foraminifer Res 20:117–127

    Article  Google Scholar 

  • Brandt K (1881) Über das Zusammenleben von Algen und Tieren. Biol Zentbl 1:524–527

    Google Scholar 

  • 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 132:349–355

    Article  Google Scholar 

  • Cachon M, Caram B (1979) A symbiotic green alga, Pedinomonas symbiotica sp. nov. (Prasinophyceae), in the radiolarian Thalassolampe margarodes. Phycologia 18:177–184

    Article  Google Scholar 

  • Caron DA, Swanberg NR (1990) The ecology of planktonic sarcodines. Rev Aquat Sci 3:147–180

    Google Scholar 

  • 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 17:103–129

    Article  Google Scholar 

  • Carpenter EJ, Foster RA (2002) Marine cyanobacterial symbioses. In: Rai A, Bergman B, Rasmussan U (eds) Cyanobacteria in symbiosis. Kluwer Publishers, Dordrecht, pp 11–17

    Google Scholar 

  • Carpenter EJ, Janson S (2000) Intracellular cyanobacterial symbionts in the marine diatom Climacodium frauenfeldianum (Bacillariophyceae). J Phycol 36:540–544

    Article  Google Scholar 

  • 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 159–165

    Google Scholar 

  • Chesnick JM, Cox ER (1987) Synchronized sexuality of an algal symbiont and its dinoflagellate host, Peridinium balticum (Levander) Lemmermann. Biosystems 21:69–78

    Article  CAS  PubMed  Google Scholar 

  • 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 164:411–422

    Article  CAS  PubMed  Google Scholar 

  • de Bary AH (1878) Ueber Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher und Aerzte in Cassel. Baier & Lewalter, Kassel, pp 121–126

    Google Scholar 

  • Decelle J (2013) New perspectives on the functioning and evolution of photosymbiosis in plankton: mutualism or parasitism? Commun Integr Biol 6(4):e24560

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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 109:18000–18005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Decelle J, Siano R, Probert I et al (2012b) Multiple microalgal partners in symbiosis with the acantharian Acanthochiasma sp. (Radiolaria). Symbiosis 58:233–244

    Article  CAS  Google Scholar 

  • Decelle J, Suzuki N, Mahé F et al (2012c) Molecular phylogeny and morphological evolution of the Acantharia (Radiolaria). Protist 163:435–450

    Article  PubMed  Google Scholar 

  • Dufrêne YF (2002) Atomic force microscopy, a powerful tool in microbiology. J Bacteriol 184:5205–5213

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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 315–335

    Google Scholar 

  • Erickson JS, Hashemi N, Sullivan JM et al (2012) In situ phytoplankton analysis: there’s plenty of room at the bottom. Anal Chem 84:839–850

    Article  CAS  PubMed  Google Scholar 

  • Escalera L, Reguera B, Takishita K et al (2011) Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae). Protist 162:304–311

    Article  PubMed  Google Scholar 

  • 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 18:334–343

    Article  Google Scholar 

  • Fairbanks RG, Wiebe PH (1980) Foraminifera and chlorophyll maximum: vertical distribution, seasonal succession, and paleoceanographic significance. Science 209:1524–1526

    Article  CAS  PubMed  Google Scholar 

  • 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 61:105–117

    Article  Google Scholar 

  • 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 59:215–226

    Article  Google Scholar 

  • 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 160:285–300

    Article  PubMed  Google Scholar 

  • Foissner W, Berger H, Schaumburg J (1999) Identification and ecology of limnetic plankton ciliates. Bavarian State Office for Water Management, Munich

    Google Scholar 

  • 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 1197–1218

    Chapter  Google Scholar 

  • Foster RA, Zehr JP (2006) Characterization of diatom-cyanobacteria symbioses on the basis of nifH, hetR, and 16S rRNA sequences. Environ Microbiol 8:1913–1925

    Article  CAS  PubMed  Google Scholar 

  • 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 42:453–463

    Article  CAS  Google Scholar 

  • 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 42:243–250

    Article  CAS  Google Scholar 

  • 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 46:1028–1037

    Article  CAS  Google Scholar 

  • Foster RA, Kupyers MMM, Vagner T et al (2011) Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5:1484–1493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frada M, Young M, Cachão M et al (2010) A guide to extant coccolithophores (Calcihaptophycidae, Haptophyta) using light microscopy. J Nannoplankton Res 31:58–112

    Google Scholar 

  • Frank AB (1877) Über die biologischen Verhältnisse des Thallus einiger Krusten-Flechten. Beitr Biol Pflanz 2:132–200

    Google Scholar 

  • 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 36:1403–1407

    Article  Google Scholar 

  • Fukuda Y, Endoh H (2006) New details from the complete life cycle of the red-tide dinoflagellate Noctiluca scintillans (Ehrenberg) McCartney. Eur J Protistol 42:209–219

    Article  PubMed  Google Scholar 

  • Gast RJ, Caron DA (1996) Molecular phylogeny of symbiotic dinoflagellates from Foraminifera and Radiolaria. Mol Biol Evol 13:1192–1197

    Article  CAS  PubMed  Google Scholar 

  • Gast RJ, Caron DA (2001) Photosymbiotic associations in planktonic Foraminifera and Radiolaria. Hydrobiologia 461:1–7

    Article  Google Scholar 

  • Gast RJ, McDonnell TA, Caron DA (2000) srDNA-based taxonomic affinities of algal symbionts from a planktonic foraminifer and a solitary radiolarian. J Phycol 36:172–177

    Article  Google Scholar 

  • Gast RJ, Moran DM, Dennett MR et al (2007) Kleptoplastidy in an Antarctic dinoflagellate: caught in evolutionary transition? Environ Microbiol 9:39–45

    Article  CAS  PubMed  Google Scholar 

  • Gast RJ, Sanders RW, Caron DA (2009) Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol 17:563–569

    Article  CAS  PubMed  Google Scholar 

  • Geddes P (1878) Sur la fonction de la chlorophylle avec les planaires vertes. CR Séances Acad Sci Paris 87:1095–1097

    Google Scholar 

  • Gómez F (2007) The consortium of the Protozoan Solenicola setigera and the diatom Leptocylindrus mediterraneus in the Pacific Ocean. Acta Protozool 46:15–24

    Google Scholar 

  • Gómez F, Moreira D, López-García P (2010) Molecular phylogeny of the dinoflagellates Podolampas and Blepharocysta (Peridiniales, Dinophyceae). Phycologia 49:212–220

    Article  Google Scholar 

  • 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 47:393–406

    Article  Google Scholar 

  • 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 18:1–1803

    Google Scholar 

  • 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:e81749

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hansen PJ (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J Eukaryot Microbiol 58:203–214

    Article  CAS  PubMed  Google Scholar 

  • Hansen PJ, Fenchel T (2006) The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar Biol Res 2:169–177

    Article  Google Scholar 

  • Hansen PJ, Miranda L, Azanza R (2004) Green Noctiluca scintillans: a dinoflagellate with its own greenhouse. Mar Ecol Prog Ser 275:79–87

    Article  CAS  Google Scholar 

  • Harrison PJ, Furuya K, Glibert PM et al (2011) Geographical distribution of red and green Noctiluca scintillans. Chin J Oceanol Limnol 29:807–831

    Article  Google Scholar 

  • Hasle GR (1975) Some living marine species of the diatom family Rhizosoleniaceae. Nova Hedwig Beih 53:99–140

    Google Scholar 

  • Hemleben C, Spindler M (1983) Recent advances in research on living planktonic Foraminifera. Utrecht Micropalaeontol Bull 30:141–170

    Google Scholar 

  • Hemleben C, Spindler M, Anderson OR (1989) Modern planktonic Foraminifera. Springer, Heidelberg

    Book  Google Scholar 

  • 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):774–791

    Article  Google Scholar 

  • Hilton JA, Foster RA, Tripp HJ et al (2013) Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont. Nat Commun 4:1767

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hirose E, Hirabayashi S, Hori K et al (2006) UV protection in the photosymbiotic ascidian Didemnum molle inhabiting different depths. Zool Sci 23:57–63

    Article  CAS  PubMed  Google Scholar 

  • 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 127–132

    Google Scholar 

  • Huxley TH (1851) Upon Thalassicolla, a new zoophyte. Ann Mag Nat Hist Ser 2 8:433–442

    Google Scholar 

  • Imanian B, Keeling PJ (2007) The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages. BMC Evol Biol 7:172

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Imanian B, Pombert JF, Keeling PJ (2010) The complete plastid genomes of the two ‘dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum. PloS One 5:e10711

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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 201:121–128

    Article  Google Scholar 

  • 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 34:171–176

    Article  Google Scholar 

  • Janson S, Wouters J, Bergman B et al (1999) Host specificity in the Richelia-diatom symbiosis revealed by hetR gene sequence analysis. Environ Microbiol 1:431–438

    Article  CAS  PubMed  Google Scholar 

  • Johnson MD (2011) Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J Eukaryot Microbiol 58:185–195

    Article  PubMed  Google Scholar 

  • Jørgensen BB, Erez J, Revsbech NP et al (1985) Symbiotic photosynthesis in a planktonic foraminiferan, Globigerinoides sacculifer (Brady), studied with microelectrodes. Limnol Oceanogr 30:1253–1267

    Article  Google Scholar 

  • 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 33–77

    Google Scholar 

  • 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 36:259–271

    Article  CAS  PubMed  Google Scholar 

  • Lampitt RS, Salter I, John D (2009) Radiolaria: major exporters of organic carbon to the deep ocean. Global Biogeochem Cycles 23:GB1010

    Article  CAS  Google Scholar 

  • Lee JJ (2006) Algal symbiosis in larger Foraminifera. Symbiosis 42:63–75

    Google Scholar 

  • 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 141:207–208

    Article  Google Scholar 

  • Lombard F, Labeyrie L, Michel E et al (2009) Modelling the temperature dependent growth rates of planktic Foraminifera. Mar Micropaleontol 70:1–7

    Article  Google Scholar 

  • Lucas IAN (1991) Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia 33:213–224

    Article  Google Scholar 

  • 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 8:182–188

    Article  Google Scholar 

  • Malfatti F, Azam F (2009) Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat Microb Ecol 58:1–14

    Article  Google Scholar 

  • 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:263–275

    Article  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven

    Google Scholar 

  • Massera Bottazzi E, Andreoli MG (1981) “Blooming” of Acantharia (Protozoa-Sarcodina) in the southern Atlantic Ocean. Quad Lab Technol 3:637

    Google Scholar 

  • Mayali X, Weber PK, Brodie EL et al (2012) High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use. ISME J 6:1210–1221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Michaels AF (1988) Vertical distribution and abundance of Acantharia and their symbionts. Mar Biol 97:559–569

    Article  Google Scholar 

  • Michaels AF (1991) Acantharian abundance and symbiont productivity at the VERTEX seasonal station. J Plankton Res 13:399–418

    Article  Google Scholar 

  • 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 17:131–163

    Article  Google Scholar 

  • Moisander PH, Beinhart RA, Hewson I et al (2010) Unicellular cyanobacterial distributions broaden oceanic N2 fixation domain. Science 327:1512–1514

    Article  CAS  PubMed  Google Scholar 

  • Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518

    Article  CAS  PubMed  Google Scholar 

  • Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104:8627–8633

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 209:3413–3419

    Article  CAS  PubMed  Google Scholar 

  • Müller J (1858) Über die Thalassicollen, Polycystinen und Acanthometren des Mittelmeeres. Abh Königl Preuß AkadWiss, Berlin, pp 1–62

    Google Scholar 

  • Murray J (1897) On the distribution of the pelagic Foraminifera at the surface and on the floor of the ocean. Nat Sci (Ecol) 11:17–27

    Google Scholar 

  • 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 105:17861–17866

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Musat N, Foster RA, Vagner T et al (2011) Detecting metabolic activities in single cells with emphasis on nanoSIMS. FEMS Microbiol Rev 36:486–511

    Article  PubMed  CAS  Google Scholar 

  • 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 166–176

    Google Scholar 

  • Olson RJ, Sosik HM (2007) A submersible imaging-in-flow instrument to analyze nano- and microplankton: imaging FlowCytobot. Limnol Oceanogr Methods 5:195–203

    Article  Google Scholar 

  • 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 56:97–101

    Article  Google Scholar 

  • Parke M, Manton I (1967) Specific identity of algal symbiont in Convoluta roscoffensis. J Mar Biol Assoc UK 47:445–457

    Article  Google Scholar 

  • Pedrós-Alió C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4:449–466

    Article  PubMed  Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid Foraminifera in Hawaii. Mol Phylogenet Evol 56:492–497

    Article  CAS  PubMed  Google Scholar 

  • 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 50:388–399

    Article  CAS  Google Scholar 

  • Rampi L (1952) Ricerche sul Microplancton di superficie del Pacifico tropicale. Bull Inst Océanogr (Monaco) 1014:1–16

    Google Scholar 

  • Rink S, Kühl M, Bijma J et al (1998) Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa. Mar Biol 131:583–595

    Article  Google Scholar 

  • Rodenacker K, Hense B, Jütting U et al (2006) Automatic analysis of aqueous specimens for phytoplankton structure recognition and population estimation. Microsc Res Tech 69:708–720

    Article  PubMed  Google Scholar 

  • Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202–209

    Article  PubMed  Google Scholar 

  • Schewiakoff WT (1926) The Acantharia. Fauna e Flora del Golfo di Napoli 37:1–755

    Google Scholar 

  • Schoemann V, Becquevort S, Stefels J et al (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53:43–66

    Article  CAS  Google Scholar 

  • Schulze K, Tillich UM, Dandekar T et al (2013) PlanktoVision – an automated analysis system for the identification of phytoplankton. BMC Bioinformatics 14:115

    Article  PubMed Central  PubMed  Google Scholar 

  • Schütt F (1895) Die Peridineen der Plankton-Expedition. Ergeb Plankton-Exped Humboldt-Stifung 4:1–170

    Google Scholar 

  • Schweikert M, Elbrächter M (2004) First ultrastructural investigations of the consortium between a phototrophic eukaryotic endocytobiont and Podolampas bipes (Dinophyceae). Phycologia 43:614–623

    Article  Google Scholar 

  • Schwendener S (1868) Untersuchungen über den Flechtenthallus. Beitr Wiss Bot 6:195–207

    Google Scholar 

  • 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 325:59–71

    Article  CAS  Google Scholar 

  • 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 15:1441–1451

    Article  PubMed  CAS  Google Scholar 

  • Siano R, Montresor M, Probert I et al (2010) Pelagodinium gen. nov and P. béii comb. nov., a dinoflagellate symbiont of planktonic Foraminifera. Protist 161:385–399

    Article  PubMed  Google Scholar 

  • Sournia A (1986) Atlas du phytoplancton marin. I. Cyanophycees, Dictyophycees, Dinophycees et Raphidophycees, vol 1. CNRS, Paris, pp 1–219

    Google Scholar 

  • Spero HJ (1987) Symbiosis in the planktonic foraminifer, Orbulina universa, and the isolation of its symbiotic dinoflagellate Gymnodinium béii sp. nov. J Phycol 23:307–317

    Article  Google Scholar 

  • Spero HJ, Angel DL (1991) Planktonic sarcodines: microhabitat for oceanic dinoflagellates. J Phycol 27:187–195

    Article  Google Scholar 

  • Spindler M, Hemleben C, Bayer U et al (1979) Lunar periodicity of reproduction in the planktonic foraminifer Hastigerina pelagica. Mar Ecol Prog Ser 1:61–64

    Article  Google Scholar 

  • Stoecker DK, Silver MW, Michaels AE (1988–1989) Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Mar Microb Food Webs 3:79–100

    Google Scholar 

  • Stoecker DK, Gustafson DE, Verity PG (1996) Micro- and mesoprotozooplankton at 140°W in the equatorial Pacific: heterotrophs and mixotrophs. Aquat Microb Ecol 10:273–282

    Article  Google Scholar 

  • Stoecker DK, Johnson MD, de Vargas C et al (2009) Acquired phototrophy in aquatic protists. Aquat Microb Ecol 57:279–310

    Article  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP et al (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  CAS  PubMed  Google Scholar 

  • 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 35:169–182

    Google Scholar 

  • Swanberg NR, Caron DA (1991) Patterns of sarcodine feeding in epipelagic oceanic plankton. J Plankton Res 13:287–322

    Article  Google Scholar 

  • Sweeney BM (1976) Pedinomonas noctilucae (Prasinophyceae), the flagellate symbiotic in Noctiluca (Dinophyceae) in Southeast Asia. J Phycol 12:460–464

    Google Scholar 

  • Sweeney BM (1978) Ultrastructure of Noctiluca miliaris (Pyrrophyta) with green flagellate symbionts. J Phycol 14:116–120

    Article  Google Scholar 

  • Takahashi O, Mayama S, Matsuoka A (2003) Host-symbiont associations of polycystine Radiolaria: epifluorescence microscopic observation of living Radiolaria. Mar Micropaleontol 49:187–194

    Article  Google Scholar 

  • 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 73:2306–2313

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 58:197–213

    Article  Google Scholar 

  • Taylor FJR (1982) Symbioses in marine microplankton. Ann Inst Oceanogr Paris (Nova Ser) 58:61–90

    Google Scholar 

  • Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118

    Article  CAS  PubMed  Google Scholar 

  • Thompson A, Foster RA, Krupke A et al (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337:1546

    Article  CAS  PubMed  Google Scholar 

  • 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 1:511–1110

    Google Scholar 

  • Tripp HJ, Bench SR, Turk KA et al (2010) Metabolic streamlining in an open ocean nitrogen-fixing cyanobacterium. Nature 464:90–94

    Article  CAS  PubMed  Google Scholar 

  • Van Bergeijk SA, Stal LJ (2001) Dimethylsulfoniopropionate and dimethylsulfide in the marine flatworm Convoluta roscoffensis and its algal symbiont. Mar Biol 138:209–216

    Article  Google Scholar 

  • Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 30:277–293

    Article  Google Scholar 

  • Villareal TA (1989) Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocaceae) symbiosis. Br Phycol J 24:357–365

    Article  Google Scholar 

  • Villareal TA (1990) Laboratory culture and preliminary characterization of the nitrogen-fixing Rhizosolenia-Richelia symbiosis. Mar Ecol 11:117–132

    Article  CAS  Google Scholar 

  • Webster NS, Taylor MW, Behnam F et al (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12:2070–2082

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yellowlees D, Rees TAV, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694

    Article  CAS  PubMed  Google Scholar 

  • Yost DM, Mitchelmore CL (2009) Dimethylsulfoniopropionate (DMSP) lyase activity in different strains of the symbiotic alga Symbiodinium microadriaticum. Mar Ecol Prog Ser 386:61–70

    Article  CAS  Google Scholar 

  • Yuasa T, Takahashi O (2014) Ultrastructural morphology of the reproductive swarmers of Sphaerozoum punctatum (Huxley) from the East China Sea. Eur J Protistol 50:194–204

    Article  PubMed  Google Scholar 

  • Yuasa T, Horiguchi T, Mayama S et al (2012) Ultrastructural and molecular characterization of symbionts in Dictyocoryne profunda (polycystine radiolarian). Symbiosis 57:51–55

    Article  CAS  Google Scholar 

  • Zeder M, Ellrott A, Amann R (2011) Automated sample area definition for high-throughput microscopy. Cytometry A 79A:306–310

    Article  Google Scholar 

  • Zehr JP, Waterbury JB, Turner PJ et al (2001) Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412:635–638

    Article  CAS  PubMed  Google Scholar 

  • Zehr JP, Bench SR, Carter BJ et al (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322:1110–1112

    Article  CAS  PubMed  Google Scholar 

  • Zetsche EM, Meysman FJR (2012) Dead or alive? Viability assessment of micro- and mesoplankton. J Plankton Res 34:493–509

    Article  CAS  Google Scholar 

  • 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 10:147–161

    PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johan Decelle .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Decelle, J., Colin, S., Foster, R.A. (2015). Photosymbiosis in Marine Planktonic Protists. In: Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N., Not, F. (eds) Marine Protists. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55130-0_19

Download citation

Publish with us

Policies and ethics