Symbiosis

, Volume 49, Issue 2, pp 61–70 | Cite as

The luggage hypothesis: Comparisons of two phototrophic hosts with nitrogen-fixing cyanobacteria and implications for analogous life strategies for kleptoplastids/secondary symbiosis in dinoflagellates

  • Johanna Wouters
  • John A. Raven
  • Susanna Minnhagen
  • Sven Janson
Reveiw article

Abstract

Nostoc and Richelia belong to a group of heterocystous cyanobacteria and are unique within this group in forming intracellular symbioses with phototrophic hosts, the angiosperm Gunnera and the diatoms (algae) Rhizosolenia and Hemiaulus, respectively. The function of the cyanobiont is similar in the symbioses, namely providing fixed atmospheric nitrogen to their hosts; also the cyanobionts are contained in a host compartment, the symbiosome. The evolutionary timescale for the cyanobiont-endosymbiosis formation is in both instances about ≈90 Ma. However, the potentials for further co-evolution of host and microsymbiont, are different. Nostoc is regarded as preyed upon by its host, while in the Richelia-Rhizosolenia symbiosis example the evolution towards a new type of permanent organelle is possible. It is proposed that symbiosis is ruled by divergent host strategies. In the case of Richelia-Rhizosolenia the evolution of a permanent symbiosis is linked to diatom hosts needing to carry the cyanobiont permanently, as it is not available free-living in the oceans. However, in the case of Nostoc/Gunnera, the host exploits an abundant cyanobacterial species. A model where the relative abundance of microsymbionts determines the nature of the symbiosis comes into view: If environmental ratios of host/microsymbiont are so that hosts are the dominating party, then the host has to carry the microsymbiont as luggage (vertical transmission). Likewise, if the ratio of microsymbiont is higher than host, than the host will prey on the microsymbiont (horizontal transmission). The article also discusses the retention of secondary plastids in dinoflagellates. We show that dinoflagellates are organisms that exemplify both types of strategies that is either preying or harbouring a permanent organelle. The difference from the cyanobacterial example is that only parts of the eukaryotic microsymbionts are kept, usually only the plastid. We emphasize that the dinoflagellates can obtain their plastids from various different organisms. The luggage theory offers an explanation to why some dinoflagellate species contain kleptoplastids, while others have permanent, secondary plastids and some have tertiary plastids.

Keywords

Endosymbiosis Nostoc Richelia plastid-evolution kleptoplastids secondary plastids dinoflagellates 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersson SGE (2006) The bacterial world gets smaller. Science 314:259–260PubMedGoogle Scholar
  2. Archibald JM (2006) Algal genomics: exploring the imprint of endosymbiosis. Current Biology 16:1033–1035Google Scholar
  3. Berman-Frank I, Lundgren P, Chen Y-B, Küpper H, Kolber Z, Bergman B, Falkowski PG (2001) Segregation of nitrogen fixation and oxygen photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1534–1537PubMedGoogle Scholar
  4. Bhattacharya D, Yoon HS, Hackett JD (2004) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26:50–60PubMedGoogle Scholar
  5. Bergman B (2002) The Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in Symbiosis. Kluwer Academic Publishers, Dordrecht, pp 207–232Google Scholar
  6. Carpenter EJ, Chang J, Cottrell M, Schubauer J, Paerl HW, Bebout BM, Capone DG (1990) Re-evaluation of nitrogenase oxygen-protective mechanisms in the planktonic marine cyanobacterium Trichodesmium. Marine Ecology Progress Series 65:151–158Google Scholar
  7. Carpenter EJ, Montoya JP, Burns J, Mullholland MR, Subramaniam A, Capone DG (1999) Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Marine Ecology Progress Series 185:273–283Google Scholar
  8. Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philosophical Transactions of the Royal Society of London Series BBiological Sciences 358:109–133Google Scholar
  9. Chesnick JM, Kooistra WHCF, Wellbrock U, Medlin LK (1997) Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). Journal of Eukaryotic Microbiology 44:314–320PubMedGoogle Scholar
  10. Chiu W-L, Peters GA, Levieille G, Still PC, Cousins S, Osborne B, Elhai J (2005) Nitrogen deprivation stimulates symbiotic gland development in Gunnera manicata. Plant Physiology 139:224–230PubMedGoogle Scholar
  11. Damste JSS, Muyzer G, Abbas B, Rampen SW, Massé G, Allard WG, Belt ST, Robert J-M, Rowland SR, Moldowan JM, Barbanti SM, Fago JF, Denisevich P, Dahl J, Trindade LAF, Schouten S (2004) The rise of the rhizosolenid diatoms. Science 304:584–587PubMedGoogle Scholar
  12. Deusch O, Landam G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, Martin W, Dagan T (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Molecular Biology and Evolution 25:748–761PubMedGoogle Scholar
  13. Douglas AE (1994) Symbiotic Interactions. Oxford Science Publications, Oxford, UKGoogle Scholar
  14. Douglas AE (2008) Tansley review: Conflict, cheats and the persistence of symbioses. New Phytologist 177:849–858PubMedGoogle Scholar
  15. Douglas AE, Raven JA (2003) Genomes at the interface between bacteria and organelles. Philosophical Transactions of the Royal Society of London B 358:5–18Google Scholar
  16. Fields SD, Rhodes RG (1991) Ingestion and retention of Chroomonas spp. (Cryptophyceae) by Gymnodinium acidotum (Dinophyceae). Journal of Phycology 27:525–529Google Scholar
  17. Foster RA, Zehr JP (2006) Characterization of diatomcyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences. Environmental Microbiology 8:1913–1925PubMedGoogle Scholar
  18. Fuller DQ, Hickey LJ (2005) Systematics and leaf architecture of the Gunneraceae. Botanical Review 71:295–353Google Scholar
  19. Garces E, Fernandez M, Penna A, Van Lenning K, Gutierrez A, Camp J, Zapata M (2006) Characterization of NW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. Journal of Phycology 42:1096–1112Google Scholar
  20. Gast RJ, Moran DM, Dennett MR, Caron DA (2006) Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environmental Microbiology 9:39–45Google Scholar
  21. Gomez F, Furuya K, Takeda S (2005) Distribution of the cyanobacterium Richelia intracellularis as an epiphyte of the diatom Chaetoceros compressus in the western Pacific Ocean. Journal of Plankton Research 27:323–330Google Scholar
  22. Grzebyk KD, Schofeild O, Vetriani C, Falkowski PG (2003) The Mesozoic radiation of eukaryotic algae: the portable plastid hypothesis. Journal of Phycology 39:259–267Google Scholar
  23. Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Current Biology 14:213–218PubMedGoogle Scholar
  24. Hansen G, Daugbjerg N, Henriksen P (2000) Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. Journal of Phycology 36:394–410Google Scholar
  25. Hansen PJ, Fenchel T (2006) The bloom-forming ciliate Mesodinium rubrum harbors a single permanent endosymbiont. Marine Biology Research 2:169–177Google Scholar
  26. Hitch CJB, Stewart WDP (1973) Nitrogen fixation by lichens in Scotland. New Phytologist 72:509–524Google Scholar
  27. Horiguchi T, Pienaar RN (1991) Ultrastructure of a marine dinoflagellate, Peridinium quinquecorne Abé (Peridiniales) from South Africa with special reference to its chrysophyte endosymbiont. Botanica Marina 34:123–131Google Scholar
  28. Horiguchi T, Pienaar RN (1992) Amphidinium latum Lebour (Dinophyceae), a sand-dwelling dinoflagellate feeding on cryptomonads. Japanese Journal of Phycology 40:353–363Google Scholar
  29. Horiguchi T, Pienaar RN (1994) Ultrastructure of a new marine sand-dwelling dinoflagellate, Gymnodinium quadrilobatum Sp-Nov (Dinophyceae) with special reference to its endosymbiotic alga. European Journal of Phycology 29:237–245Google Scholar
  30. Horiguchi T, Takano Y (2006) Serial replacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridiniales, Dinophyceae). Phycological Research 54:193–200Google Scholar
  31. Inagaki Y, Dacks JB, Doolittle WF, Watanabe KI, Ohama T (2000) Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. International Journal of Systematic and Evolutionary Microbiology 50:2075–2081PubMedGoogle Scholar
  32. Ishida K, Green BR (2002) Second and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclearencoded plastid gene by that of a haptophyte tertiary endosymbiont. Proceedings of the National Academy Sciences of the USA 99:9294–9299Google Scholar
  33. Janson S, Carpenter EJ, Bergman B (1994) Compartmentalisation of nitrogenase in a non-heterocystous cyanobacterium: Trichodesmium contortum. FEMS Microbiology Letters 118:9–14Google Scholar
  34. Janson S (2002) Cyanobacteria in symbiosis with diatoms. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer Academic Publishers, Dordrecht, pp 1–10Google Scholar
  35. Janson S, Granéli E (2003) Genetic analysis of the psbA gene from single cells indicates a cryptomonad origin of the plastid in Dinophysis (Dinophyceae). Phycologia 42:473–477CrossRefGoogle Scholar
  36. Janson S (2004) Molecular evidence that plastids in the toxinproducing dinoflagellate genus Dinophysis originate from the free-living cryptophyte Teleaulax amphioxeia. Environmental Microbiology 6:1102–1106PubMedGoogle Scholar
  37. Janson S, Wouters J, Bergman B, Carpenter EJ (1999) Host specificity in the Richelia-diatom symbiosis revealed by hetR gene sequence analysis. Environmental Microbiology 1:431–438PubMedGoogle Scholar
  38. Jarzen DM (1980) The occurrence of Gunnera pollen in the fossil record. Biotropica 12:177–123Google Scholar
  39. Johansson, C. 1994. Establishment of the Gunnera-Nostoc symbiosis. Doctoral Thesis, Stockholm University (Sweden).Google Scholar
  40. Johnson MD, Oldbach D, Delwiche CF, Stoecker DH (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–428PubMedGoogle Scholar
  41. Kaiser D (2001) Building a multicelular organism. Annual Review of Genetics 35:103–123PubMedGoogle Scholar
  42. Karsten G (1907) Das Indische Phytoplankton nach dem Material der Deutschen Tiefsee-Expedition 1898–1899. Deutsche Tiefsee-Expedition 1898–1899(2):423–548Google Scholar
  43. Kühn S, Raven JA (2008) Photosynthetic oscillations in individual cells of the marine diatom Coscinodiscus wailesii (Bacillariophyceae) revealed by microsensor measurements. Photosynthesis Research 95:37–44PubMedGoogle Scholar
  44. Larsen J (1988) An ultrastructural study of Amphidinium poecilochroum (Dinophyceae), a phagotrophic dinoflagellate feeding on small species of cryptophytes. Phycologia 27:366–377Google Scholar
  45. Leister D (2003) Chloroplast research in the genomic age. Trends in Genetics 19:47–56PubMedGoogle Scholar
  46. Lewitus AJ, Glasgow HB, Burkholder JM (1999) Kleptoplastidy in the toxic dinoflagellate Pfiesteria piscicida (Dinophyceae). Journal of Phycology 35:303–312Google Scholar
  47. Lucas IAN (1991) Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia 33:213–224Google Scholar
  48. Mague TH, Weare NM, Holm-Hansen O (1974) Nitrogen fixation in the North Pacific Ocean. Marine Biology 24:109–119Google Scholar
  49. Marin N, Nowack ECM, Melkonian M (2005) A plastid in the making: primary endosymbiosis. Protist 156:425–432PubMedGoogle Scholar
  50. Margulis L, Schwartz KV (1998) Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth. W.H. Freeman & Company, New York 520 pGoogle Scholar
  51. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceedings of the National Academy of Sciences USA 99:12246–12251Google Scholar
  52. Martinez L, Silver MW, King JM, Alldredge AL (1983) Nitrogen fixation by floating diatom mats: A source of new nitrogen to oligotrophic ocean waters. Science 221:152–154PubMedGoogle Scholar
  53. Mereschowski C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biologisches Zentralblatt 25:593–604Google Scholar
  54. Minnhagen S, Janson S (2006) Genetic analyses of Dinophysis spp. support kleptoplastidy. FEMS Microbiology Ecology 57:47–54PubMedGoogle Scholar
  55. Moore RB, Obornık M, Janouskovec J, Chrudimsky T, Vancova M, Green DH, Wright SW, Davies NW, Bolch CJS, Heimann K, Slapeta J, Hoegh-Guldberg O, Logsdon JM Jr, Carter DA (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963PubMedGoogle Scholar
  56. Moustafa A, Bhattacharya D (2008) Phylosort: a userfriendly sorting tool and its application to estimating the cyanobacterial contribution to the nuclear genome of Chlamydomonas. BMC Evolutionary Biology 8:6. doi:10.11.1186/1471-2148-8-6 PubMedGoogle Scholar
  57. Nakabachi A, Yamshita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267PubMedGoogle Scholar
  58. Nowack ECM, Melkonian M, Glöckner G (2008) Chromatophores genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Current Biology 18:410–418PubMedGoogle Scholar
  59. Osborne BA, Cullen A, Jones PW, Campbell GJ (1992) Use of nitrogen by the Nostoc-Gunnera tinctoria (Molina) Mirbel symbiosis. New Phytologist 120:481–487Google Scholar
  60. Osborne B, Doris F, Cullen A, McDonald R, Campbell G, Steer M (1991) Gunnera tinctoria: an unusual nitrogenfixing invader. Bioscience 41:224–234Google Scholar
  61. Osborne BA, Sprent JI (2002) Ecology of the Nostoc-Gunnera symbiosis. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in Symbiosis. Kluwer Academic Publishers, Dordrecht, pp 233–251Google Scholar
  62. Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? Journal of Phycology 39:4–11Google Scholar
  63. Park MG, Kim S, Kim HS, Myung G, Kang YG, Yih W (2006) First successful culture of the marine dinoflagellate Dinophysis acuminate. Aquatic Microbial Ecology 45:101–106Google Scholar
  64. Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Current Opinion in Plant Biology 3:320–328PubMedGoogle Scholar
  65. Patron NJ, Rogers M, Keeling PJ (2006) Comparative rates of evolution in endosymbotic nuclear genomes. BMC Evolutionary Biology 6:46PubMedGoogle Scholar
  66. Pérez-Brocal V, Gil R, Tamos S, Lamelas A, Postigo M, Michelana JM, Silva FJ, Moya A, Latorre A (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314:312–313PubMedGoogle Scholar
  67. Pienaar RN, Sakai H, Horiguchi T (2007) Description of a new dinoflagellate with a diatom endosymbiont, Durinska capensis sp nov (Peridiniales, Dinophyceae) from South Africa. Journal of Plant Research 120:247–258PubMedGoogle Scholar
  68. Potts M (2000) Nostoc. In: Whitton BA, Potts M (eds) The Ecology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 465–504Google Scholar
  69. Prufert-Bebout L, Paerl H, Lassen C (1993) Growth, nitrogen fixation and spectral attenuation in cultivated Trichodesmium species. Applied and Evironmental Microbiology 59:1367–1375Google Scholar
  70. Rasmussen U, Svenning MM (2001) Characterisation by genotypic methods of symbiotic Nostoc strains isolated from five species of Gunnera. Archives of Microbiology 176:204–210PubMedGoogle Scholar
  71. Rasmussen U, Johansson C, Bergman B (1994) Early communication in the Gunnera-Nostoc symbiosis: plant induced cell differentiation and protein synthesis in the cyanobacterium. Molecular Plant-Microbe Interactions 7:696–702Google Scholar
  72. Raven JA, Larkum AWD (2007) Are the ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations? Photosynthesis Research 94:31–42PubMedGoogle Scholar
  73. Raven JA, Johnston AM, Handley LL, McInroy SG (1990) Transport and assimilation of inorganic carbon by Lichina pygmaea under emersed and submersed conditions. New Phytologist 114:401–417Google Scholar
  74. Reyes-Prieto A, Hackett JD, Soares MB, Bonaldo MF, Bhattacharya D (2006) Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Current Biology 16:2320–2325PubMedGoogle Scholar
  75. Rumpho ME, Dastow FF, Manlant JR, Lee J (2006) The Kleptoplast. In: Wise RR, Hoober KJ (eds) The Structure and Function of Plastids, Volume 23 of Photosynthesis and Respiration. Springer, Dordrecht, pp 451–473Google Scholar
  76. Schnepf E, Elbrächter M (1999) Dinophyte chloroplasts and phylogeny – a review. Grana 38:81–97Google Scholar
  77. Schnepf E, Winter S, Mollenhauer D (1989) Gymnodinium aeruginosum (Dinophyta): a blue-green dinoflagellate with a vestigial, anucleate, cryptophycean endosymbiont. Plant Systematics and Evolution 164:75–91Google Scholar
  78. Silvester WB, Smith DR (1969) Nitrogen-fixation by Nostoc-Gunnera symbiosis. Nature 224:1231Google Scholar
  79. Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45:361–402Google Scholar
  80. Skovgaard A (1998) Role of chloroplast retention in a marine dinoflagellate. Aquatic Microbial Ecology 15:293–301Google Scholar
  81. Staal M, Heysman FJR, Stal LJ (2003) Temperature excluders N2-fixing heterocystous cyanobacteria in the tropical oceans. Nature 425:504–507PubMedGoogle Scholar
  82. Stiller JW, Reel DC, Johnson JC (2003) A single origin of plastids revisited: convergent evolution in organellar genome content. Journal of Phycology 3:95–105Google Scholar
  83. Sweeney B (1978) Ultrastructure of Noctiluca miliaris (Pyrrophyta) with green flagellate symbionts. Journal of Phycology 14:116–120Google Scholar
  84. Tamura M, Shimada S, Horiguchi T (2005) Galeidinium rugatum gen. et sp nov (Dinophyceae), a new coccoid dinoflagellate with a diatom endosymbiont. Journal of Phycology 41:658–671Google Scholar
  85. Taylor FJR (1987) The Biology of Dinoflagellates, vol 21, Botanical Monographs. Blackwell Scientific Publications, Oxford, p 785Google Scholar
  86. Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF, Jakobsen KS (2000) Phylogenetic analyses indicate that the 19' hexanoyloxyfucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Molecular Biology and Evolution 17:718–729PubMedGoogle Scholar
  87. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: Molecularphylogenetic and palaeontological perspectives. Proceedings of the National Academy of Sciences of the USA 103:5442–5447PubMedGoogle Scholar
  88. Uheda E, Silvester WB (2001) The role of papillae during the infection process in Gunnera-Nostoc symbiosis. Plant Cell Physiology 42:780–783PubMedGoogle Scholar
  89. Usher KM, Bergman B, Raven JA (2007) Exploring cyanobacterial symbioses. Annual Review of Ecology, Evolution and Systematics 38:255–273Google Scholar
  90. Villareal TA (1989) Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocacaceae) symbiosis. European Journal of Phycology 24:357–365Google Scholar
  91. Wanntorp L, Wanntorp H-E, Oxelman B, Källersjö M (2001) Phylogeny of Gunnera. Plant Systematics and Evolution 226:85–107Google Scholar
  92. Wanntorp L, De Craene LPR (2005) The Gunnera flower: key to eudicot diversification or response to pollination mode? International Journal of Plant Sciences 166:945–953Google Scholar
  93. Wanntorp L, Dettman ME, Jarzen DM (2004) Tracking the Mesozoic distribution of Gunnera: comparison with the fossil pollen species Tricolpites reticulatus Cookson. Paleobotany and Palynology 132:163–174Google Scholar
  94. Watanabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with chlorophyll A- and B-containing endosymbiont. Journal of Phycology 26:741–751Google Scholar
  95. Welsh EA, Liberton M, Stöckel J, Loh T, Elvitigala T, Wang C, Wollam A, Fulton RS, Clifton SW, Jacobs JM, Aurora R, Ghosh BK, Sherman LA, Smith RD, Wilson RK, Pakrasi HB (2008) The genome of Cyanothece 51142, a unicellular dizotrophic cyanobacterium important in the marine nitrogen cycle. Proceedings of the National Academy of Sciences USA 105:15094–15099Google Scholar
  96. Wilcox LW, Wedemayer GJ (1985) Dinoflagellate with blue-green chloroplasts derived from an endosymbiotic eukaryote. Science 227:192–194PubMedGoogle Scholar
  97. Wouters J, Janson S, Bergman B (2000) The effect of exogenous carbohydrates on nitrogen fixation and hetR expression in Nostoc PCC 9229 forming symbiosis with Gunnera. Symbiosis 28:63–76Google Scholar
  98. Wouters J (2005) Heterocystous cyanobacteria living within symbiosomes: genetic and physiological aspects. University of Kalmar (Sweden), Doctoral ThesisGoogle Scholar
  99. Yoon HS, Hackett JD, Bhattacharya D (2002) A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proceedings of the National Academy of Sciences of USA 99:11724–11729Google Scholar
  100. Yoon HS, Hackett JD, Lidie KB, Van Dolah FM, Nosenko T, Bhattacharya D (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Molecular Biology and Evolution 22:1299–1308PubMedGoogle Scholar
  101. Yoon HS, Reyes-Prieto A, Melkonian M, Bhattacharya D (2006) Minimal plastid evolution in the Paulinella symbiont. Current Biology 16:670–672Google Scholar
  102. Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacreria lack oxygenic photosystem II. Science 322:1110–1112PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Johanna Wouters
    • 1
  • John A. Raven
    • 2
  • Susanna Minnhagen
    • 1
  • Sven Janson
    • 1
  1. 1.Department of Natural SciencesUniversity of KalmarKalmarSweden
  2. 2.University of DundeeDundeeUK

Personalised recommendations