Systematic and Evolution of Microorganisms: General Concepts

  • Charles-François Boudouresque
  • Pierre Caumette
  • Jean-Claude Bertrand
  • Philippe Normand
  • Télesphore Sime-Ngando


The diversity of metabolic activities is a characteristic of the microbial world. This enormous diversity needs to be structured in order to be understood, and as a result, taxonomy and systematics are constantly changing since the beginning of the history of microbiology and particularly today with the introduction in the last 20 years of phylogeny as the core of systematics. The history of concepts in systematics and classification is presented. Classification is the science of ordering microorganism groups (taxa) based on their interrelationships. Taxonomy is the discipline that defines the principles and laws of classification. Nomenclature is the science of defining and naming the taxonomic categories (species, genera, families, orders, classes, divisions, phyla, kingdoms, domains), according to their hierarchical rank. In this way, different schools of classification and bacterial systematics were developed in the twentieth century. Today, there is an international consensus based on the classification of the Bergey’s Manual revisited with the concepts of phylogeny. Through this classification, the concept of the prokaryotic world organization has evolved. From the idea of a kingdom of prokaryotes, the concept of three domains in the organization of life supported by phylogenetic trees is fully accepted today. Among these three domains, two are prokaryotic: Bacteria and Archaea. In this chapter, the role of horizontal gene transfers in the evolution of life is discussed. The origin of eukaryotes with the primary, secondary, and tertiary endosymbioses is also presented. This allows to improve or to transform the concept of the tree of life from phylogeny to full genome study.


Endosymbiosis Hierarchical classification History of systematics Life domains Microbial classification Microbial systematics Nomenclature codes Phylogeny Tree of life 


  1. Andersson GE (2006) The bacterial world gets smaller. Science 314:259–260PubMedGoogle Scholar
  2. Ané C, Burleigh JG, Mcmahon MM, Sanderson MJ (2005) Covarion structure in plastid genome evolution: a new statistical test. Mol Biol Evol 22(4):914–924PubMedGoogle Scholar
  3. Arslan D et al (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci U S A 108:17486–17491PubMedCentralPubMedGoogle Scholar
  4. Baldauf SL (2003) The deep roots of eucaryotes. Science 300:1703–1706PubMedGoogle Scholar
  5. Baldauf SL (2008) An overview of the phylogeny and diversity of eukaryotes. J Syst Evol 46(3):263–273Google Scholar
  6. Ball P (2007) Bacteria may be wiring up the soil. Nature 449:388PubMedGoogle Scholar
  7. Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (2003) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci U S A 90:6091–6094Google Scholar
  8. Bertrand J (1991) Mouvement des diatomées. I – L’équilibre dynamique chez Rhoicosphaenia abbreviata. Cryptogamie Algol 12(1):11–29Google Scholar
  9. Bertrand J (1992) Mouvement des diatomées. II – Synthèse des mouvements. Cryptogamie Algol 13(1):49–71Google Scholar
  10. Bhattacharya D, Yoon HS, Hackett JD (2003) Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 25(1): 50–60Google Scholar
  11. Bodyl A (2005) Do plastid-related characters support the chromalveolate hypothesis? J Phycol 41:712–718Google Scholar
  12. Bodyl A, Stiller JW, Mackiewicz P (2009) Chromalveolate plastids: direct descent or multiple endosymbioses? Trends Ecol Evol 24(3):119–121PubMedGoogle Scholar
  13. Bonen L, Doolittle W (1975) On the prokaryotic nature of red algal chloroplasts. Proc Natl Acad Sci U S A 72:2310–2314PubMedCentralPubMedGoogle Scholar
  14. Bornens M, Azimzadeh J (2007) Origin and evolution of the centrosome. In: Jékeli G (ed) Eukaryotic membranes and cytoskeleton: origin and evolution. Land Bioscience, Austin (Tx), pp 119–129Google Scholar
  15. Boudouresque CF, Gómez A (1995) Une approche moderne du monde végétal. Première Partie. GIS Posidonie Publishing, MarseilleGoogle Scholar
  16. Boullard B (1990) Guerre et paix dans le règne végétal. Edition Marketing, Paris, FranceGoogle Scholar
  17. Boxma B, De Graaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, Moon-van der Staay SY, Koopman WJH, van Hellemond JJ, Tielens AGM, Friedrich T, Veenhuis M, Huynen MA, Hackstein JHP (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79PubMedGoogle Scholar
  18. Boyen C, Oudot MP, Loiseaux-De Goer S (2001) Origin and evolution of plastids and mitochondria: the phylogenetic diversity of algae. Cah Biol Mar 42:11–24Google Scholar
  19. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285:1033–1036PubMedGoogle Scholar
  20. Buick R (2010) Ancient acritarchs. Nature 463:885–886PubMedGoogle Scholar
  21. Burki F, Okamoto N, Pombert JF, Keeling PJ (2012) The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc Royal Soc B 279:2246–2254Google Scholar
  22. Butterfield NJ (2000) Bangiomorpha pubescens n.gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26(3):386–404Google Scholar
  23. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212PubMedCentralPubMedGoogle Scholar
  24. Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M (2011) Tracing the origin of centrioles, cilia and flagella. J Cell Biol 194(2):165–175PubMedCentralPubMedGoogle Scholar
  25. Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? BioSystems 14:461–481PubMedGoogle Scholar
  26. Cavalier-Smith T (2002a) The neomurian origin of archaebacteria, the negibacterial root of the universal tree and the bacterial megaclassification. Int J Syst Evol Microbiol 52:7–76PubMedGoogle Scholar
  27. Cavalier-Smith T (2002b) The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int J Syst Evol Microbiol 52:295–354Google Scholar
  28. Cérémonie H, Buret F, Simonet P, Vogel TM (2004) Isolation of lightning-competent soil bacteria. Appl Environ Microbiol 70:6342–6346PubMedCentralPubMedGoogle Scholar
  29. Chadefaud M (1960) Tome I: Les végétaux non vasculaires. Cryptogamie. In: Chadefaud M. et Emberger L (eds) Traité de botanique systématique. Masson et Cie Publishing, Paris, pp –i-xv + 1–1018Google Scholar
  30. Chen M, Hiller RG, Howe CJ, Larkum AWD (2005) Unique origin and lateral transfer of prokaryotic chlorophyll-b and chlorophyll-d light harvesting systems. Mol Biol Evol 22(1):21–28PubMedGoogle Scholar
  31. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of Life. Science 311:1283–1286PubMedGoogle Scholar
  32. Claverie JM (2006) Viruses take center stage in cellular evolution. Genome Biol 7:110PubMedCentralPubMedGoogle Scholar
  33. Claverie JM, Abergel C (2009) Mimivirus and its virophage. Annu Rev Gen 43:49–66Google Scholar
  34. Claverie JM, Abergel C (2010) Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet 26:431–437PubMedGoogle Scholar
  35. Claverie JM, Otaga H, Audic S, Abergel C, Suhre K, Fournier PE (2006) Mimivirus and the emerging concept of “giant” virus. Virus Res 117:133–144PubMedGoogle Scholar
  36. Combes C (1995) Les interactions durables. Ecologie et évolution du parasitisme. Masson Publishing, ParisGoogle Scholar
  37. Combes C (2001) Les associations du vivant. L’art d’être parasite. Flammarion Publishing, ParisGoogle Scholar
  38. Courties C, Vaquer A, Troussellier M, Lautier J, Chrétiennot-Dinet MJ, Neuveux J, Machado C, Claustre H (1994) Smallest eukaryotic organism. Nature 370:255Google Scholar
  39. Curtis NE, Massey SE, Pierce SK (2006) The symbiotic chloroplasts in the Sacoglossan Elysia clarki are from several algal species. Invert Biol 125(4):336–345Google Scholar
  40. Dagan T, Martin W (2009) Seeing green and red in diatom genomes. Science 324:1651–1652PubMedGoogle Scholar
  41. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, LondonGoogle Scholar
  42. Daubin V, Gouy M, Perriere G (2001) Bacterial molecular phylogeny using supertree approach. Genome Inform Ser Workshop Genome Inform 12:155–164Google Scholar
  43. Di Giulio M (2003) The universal ancestor and the ancestor of bacteria were hyperthermophiles. J Mol Evol 57:721–730PubMedGoogle Scholar
  44. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128PubMedGoogle Scholar
  45. Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304:253–257PubMedGoogle Scholar
  46. El Albani A, Bengston S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, Hammarlund EU, Boulvais P, Dupuy JJ, Fontaine C, Fürsich FT, Gauthier-Lafay F, Janvier P, Javaux E, Ossa Ossa F, Pierson-Wickmann AC, Riboulleau A, Sardini P, Vachard D, Whitehoute M, Meunier A (2010) Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466:100–104PubMedGoogle Scholar
  47. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630PubMedGoogle Scholar
  48. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360PubMedGoogle Scholar
  49. Feldmann J, Feldmann G (1946) Recherches sur l’appareil conducteur des Floridées. Rev Cytol 8:159–209Google Scholar
  50. Fischer MG et al (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A 107:19508–19513PubMedCentralPubMedGoogle Scholar
  51. Forterre P, Philippe H (1999) The last universal common ancestor (LUCA): simple or complex? Biol Bull 196:373–375; discussion: 375–377PubMedGoogle Scholar
  52. Fox GE, Stackbrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen B, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463PubMedGoogle Scholar
  53. Galtier N, Tourasse N, Gouy M (1999) A nonhyperthermophilic common ancestor to extant life forms. Science 283:220–221PubMedGoogle Scholar
  54. Germot A, Philippe H, Le Guyader H (1997) Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasit 87:159–168Google Scholar
  55. Gorenflot R, Guern M (1989) Organisation et biologie des Thallophytes. Doin Publishing, ParisGoogle Scholar
  56. Green BR (2005) Lateral gene transfer in the cyanobacteria: chlorophylls, proteins and scraps of ribosomal RNA. J Phycol 41:449–452Google Scholar
  57. Haeckel E (1894) Systematische Phylogenie. Entwurf eines naturlichen Systems der Organismen auf Grund ihrer Stammesgeschichte. Erster Theil, Systematische Phylogenie der Protisten und Pflanzen. Georg Reimer, Berlin/AllemagneGoogle Scholar
  58. Hansen PJ, Fenchel T (2006) The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar Biol Res 2:169–177Google Scholar
  59. Häring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D (2005) Independent virus development outside a host. Nature 436:1101–1102Google Scholar
  60. Hébant C (1977) The conducting tissues of bryophytes. Bryophytorum Bibl 10:1–157 + 80 pl. h.tGoogle Scholar
  61. Hrdy I, Hirt RP, Dolezal P, Bardonová L, Foster PG, Tachezy J, Embley TM (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618–622PubMedGoogle Scholar
  62. Huber H, Hohn MJ, Rachel R, Fuchs T, Wimmer VC, Stetter KO (2002) A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417:63–67PubMedGoogle Scholar
  63. Jeon KW (1972) Development of cellular dependence on infective organisms: microsurgical studies in amoebas. Science 176:1122–1123PubMedGoogle Scholar
  64. Jeon KW (1991) Amoeba and x-bacteria: symbiont acquisition and possible species change. In: Margulis L, et Fester R (eds) Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. MIT Press, Cambridge, USA, pp 118–131Google Scholar
  65. Jeon KW (1995) Bacterial endosymbiosis in amoebae. Trends Cell Biol 5:137–140PubMedGoogle Scholar
  66. Jeon KW, Jeon MS (1976) Endosymbiosis in amoeba : recently established endosymbionts have become required cytoplasmic components. J Cell Physiol 89(2):337–344PubMedGoogle Scholar
  67. Johnson MD, Oldach D, Delwiche CF, Stoecker DK (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–428PubMedGoogle Scholar
  68. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okamura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–116, 185–209PubMedGoogle Scholar
  69. Kim GH, Yoon M, Klotchkova TA (2005) A moving mat: phototaxis in the filamentous green algae Spirogyra (Chlorophyta, Zygnemataceae). J Phycol 41:232–237Google Scholar
  70. Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626PubMedGoogle Scholar
  71. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJM, Palmer JD, Roos DS (1997) A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485–1489PubMedGoogle Scholar
  72. Kozo-Polyanski BM (1924) A new principle of biology. Essay on the theory of symbiogenesis. Moscou, Russie (en russe)Google Scholar
  73. Kumar S (2005) Molecular clocks: four decades of evolution. Nat Rev Genet 6(8):654–662PubMedGoogle Scholar
  74. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D (2003) A giant virus in amoebae. Science 299:2033PubMedGoogle Scholar
  75. Lamarck JB (1809) Philosophie zoologique. Dentu, ParisGoogle Scholar
  76. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 95(16):9413–9417PubMedCentralPubMedGoogle Scholar
  77. Leander BS, Saldarriaga JF, Keeling PJ (2002) Surface morphology of the marine parasite Haplozoon axiothellae Siebert (Dinoflagellata). Eur J Protistol 38:287–297Google Scholar
  78. Lecointre G, Le Guyader H (2001) Classification phylogénétique du vivant. Belin Publishing, ParisGoogle Scholar
  79. Lecointre G, Le Guyader H (2006) Classification phylogénétique du vivant, 3rd edn. Belin Publishing, ParisGoogle Scholar
  80. Lee RE, Kugrens P (2000) Ancient atmospheric CO2 and the timing of evolution of secondary endosymbioses. Phycologia 39(2): 167–172Google Scholar
  81. Lewin RA (1975) A marine Synechocystis (Cyanophyta, Chlorococcales) epizoic on ascidians. Phycologia 14:153–160Google Scholar
  82. Lewin RA (1976) Prochlorophyta as a proposed new division of algae. Nature 261:687–698Google Scholar
  83. Lewin RA, Withers N (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256:735–737Google Scholar
  84. Linnaeus C (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Holmiae, Impensis Laurentii Salvii, StockholmGoogle Scholar
  85. López-García P, Rodríguez-Valera F, Pedrós-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607PubMedGoogle Scholar
  86. Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven/LondonGoogle Scholar
  87. Margulis L (1980) Undulipodium, flagella and cilia. BioSystems 12(1–2):105–108PubMedGoogle Scholar
  88. Margulis L (1981) Symbiosis in cell evolution. W.H. Freeman, San FranciscoGoogle Scholar
  89. Margulis L, Dolan MF, Guerrero R (2000) The chimeric eukaryote: origin of the nucleus from the karyomastigont in amitochondriate protists. Proc Natl Acad Sci U S A 97:6954–6959PubMedCentralPubMedGoogle Scholar
  90. 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. Proc Natl Acad Sci U S A 99:12246–12251PubMedCentralPubMedGoogle Scholar
  91. McCutcheon JP, Moran NA (2011) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol, 14 ppGoogle Scholar
  92. McFadden GI (2001) Primary and secondary endosymbiosis and the origin of plastids. J Phycol 37:951–959Google Scholar
  93. McFadden GI, Waller RF (1997) Plastids in parasites of humans. Bioessays 19(11):1033–1040PubMedGoogle Scholar
  94. Medlin LK, Kaczmarska I (2004) Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43(3):245–270Google Scholar
  95. Mereschkowsky C (1905) ÜberNatur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Zentralbl 25:593–604Google Scholar
  96. Mereschkowsky C (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol Zentralbl 30:278–367Google Scholar
  97. Meyerowitz EM (2002) Plants compared to animals: the broadest comparative study of development. Science 295:1482–1485PubMedGoogle Scholar
  98. Monier A, Claverie JM, Ogata H (2008) Taxonomic distribution of large DNA viruses in the sea. Genome Biol 9:R106PubMedCentralPubMedGoogle Scholar
  99. Moon-van der Staay SY, De Wachter R, Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607–610PubMedGoogle Scholar
  100. Moustafa A, Beszteri B, Maier UW, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in Diatoms. Science 324:1724–1726PubMedGoogle Scholar
  101. Nakabachi A, Yamashita 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
  102. Nakayama T, Ishida K (2005) Another primary endosymbiosis? Origin of Paulinella chromatophora cyanelles. Phycologia 44(4):74Google Scholar
  103. Nicolaev SI, Berney C, Fahrni JF, Bolivar I, Polet S, Mylnikov AP, Aleshin VV, Petrov NB, Pawlowski J (2004) The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc Natl Acad Sci U S A 101(21):8066–8071Google Scholar
  104. Nishikawa M, Suzuki K, Yoshida K (1992) DNA integration into recipient yeast chromosomes by trans-kingdom conjugation between Escherichia coli and Saccharomyces cerevisiae. Curr Genet 21:101–108PubMedGoogle Scholar
  105. Oltmanns F (1904) Morphologie und Biologie der Algen. Erster Band. Gustav Fischer, JenaGoogle Scholar
  106. Pennisi E (2006) Plant wannabes. Science 313:1229PubMedGoogle Scholar
  107. Polzin KM, McKay LL (1991) Identification, DNA sequence, and distribution of IS981, a new, high-copy-number insertion sequence in lactococci. Appl Environ Microbiol 57:734–743PubMedCentralPubMedGoogle Scholar
  108. Rahat M, Ben Ishac-Monselise E (1979) Photobiology of the chloroplast hosting mollusc Elysia timida (Opisthobranchia). J Exp Mar Biol Ecol 79:225–233Google Scholar
  109. Raoult D, Audio S, Robert C, Abergel C, Ernesto P, Ogata H, La Scola B, Suzan M, Claverie JM (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350PubMedGoogle Scholar
  110. Raven PH (1970) A multiple origin for plastids and mitochondria. Science 169:641–646PubMedGoogle Scholar
  111. Raven JA, Richardson K (1984) Dinophyte flagella: a cost-benefit analysis. New Phytol 98:259–276Google Scholar
  112. Raven JA, Waite AM (2004) The evolution of silicification in diatoms: inescapable sinking and sinking as escape? New Phytol 162:45–61Google Scholar
  113. Reith M, Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5:465–475PubMedCentralPubMedGoogle Scholar
  114. Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155PubMedGoogle Scholar
  115. Rumpho ME, Summer EJ, Manhart JR (2000) Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol 123:29–38PubMedCentralPubMedGoogle Scholar
  116. Rumpho ME, Worful JM, Lee J, Kannan K, Tyler MS, Bhattacharya D, Moustafa A, Manhart JR (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc Natl Acad Sci U S A 105(46):17867–17871PubMedCentralPubMedGoogle Scholar
  117. Santini S, Jeudy S, Bartoli J, Poirot O, Lescot M, Abergel C, Barbe V, Wommack KE, Noordeloos AAM, Brussaard CPD, Claverie JM (2013) The genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc Natl Acad Sci U S A 110(26):10800–10805Google Scholar
  118. Schulz HN, Brinkhoff T, Ferdelman TG, Hernández Mariné M, Teske A, Jørgensen BB (1999) Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284:493–495PubMedGoogle Scholar
  119. Selga T, Selga M, Gobiņš V, Ozoliņa A (2010) Plastid-nuclear complexes: permanent structures in photosynthesizing tissues of vascular plants. Environ Exp Biol 8:85–92Google Scholar
  120. Smith M, Hansen J (2007) Interaction between Mesodinium rubrum and its prey: importance of prey concentration, irradiance and pH. Mar Ecol Prog Ser 338:61–70Google Scholar
  121. Stacey G, Bottomley PJ, Van Baalen C, Tabita FR (1979) Control of heterocyst and nitrogenase synthesis in cyanobacteria. J Bacteriol 137:321–326PubMedCentralPubMedGoogle Scholar
  122. Stanier RY (1974) Division I, the Cyanobacteria. In: Buchanan RE, et Gibbons NE (eds) Bergey’s manual of determinative bacteriology. Williams & Wilkins Co, BaltimoreGoogle Scholar
  123. Stiller JW, Reel DC, Johnson JC (2003) A single origin of plastids revisited : convergent evolution in organellar genome content. J Phycol 39:95–105Google Scholar
  124. Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338PubMedGoogle Scholar
  125. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL et al (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266PubMedGoogle Scholar
  126. Vaulot D, Eikrem W, Viprey M, Moreau H (2008) The diversity of small eukaryotic phytoplankton (<or =3 micron) in marine Ecosystems. FEMS Microbiol Rev 32:795–820PubMedGoogle Scholar
  127. Waggoner B (2001) Eukaryotes and multicells: origin. In: Encyclopedia of life sciences. Macmillan Publishing Ltd, Basingstoke, pp 1–9Google Scholar
  128. Williams SI, Walker DI (1999) Mesoherbivore-macroalagal interactions: feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanogr Mar Biol Annu Rev 37:87–128Google Scholar
  129. Woese C (1977) Endosymbionts and mitochondrial origins. J Mol Evol 10:39–96Google Scholar
  130. Woese CR, Olsen GJ (1986) Archaebacterial phylogeny: perspectives on the urkingdoms. Syst Appl Microbiol 7:161–177Google Scholar
  131. Worden AZ, Nolan JK, Palenik B (2004) Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 49:168–179Google Scholar
  132. Yoosuf N et al (2012) Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga Moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Gen Biol Evol 4:1324–1330Google Scholar
  133. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, et Vogel HJ (eds) Evolving genes and proteins. Academic, New York, pp 97–166Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Charles-François Boudouresque
    • 1
  • Pierre Caumette
    • 2
  • Jean-Claude Bertrand
    • 1
  • Philippe Normand
    • 3
  • Télesphore Sime-Ngando
    • 4
  1. 1.Institut Méditerranéen d’Océanologie (MIO)UM 110, CNRS 7294 IRD 235, Université de Toulon, Aix-Marseille UniversitéMarseille Cedex 9France
  2. 2.Institut des Sciences Analytiques et de Physico-chimie pour l’Environnement et les Matériaux (IPREM)UMR CNRS 5254, Université de Pau et des Pays de l’AdourPau CedexFrance
  3. 3.Microbial Ecology CenterUMR CNRS 5557 / USC INRA 1364, Université Lyon 1VilleurbanneFrance
  4. 4.Laboratoire Microorganismes: Génome et Environnement (LMGE)UMR CNRS 6023, Université Blaise Pascal, Clermont UniversitéAubère CedexFrance

Personalised recommendations