Biology & Philosophy

, Volume 31, Issue 4, pp 571–589 | Cite as

Molecular organisms

John Archibald, One Plus One Equals One: Symbiosis and the Origin of Complex Life. Oxford: Oxford University Press, 2014
  • Maureen A. O’Malley
Review Essay


Protistology, and evolutionary protistology in particular, is experiencing a golden research era. It is an extended one that can be dated back to the 1970s, which is when the molecular rebirth of microbial phylogeny began in earnest. John Archibald, a professor of evolutionary microbiology at Dalhousie University (Nova Scotia, Canada), focuses on the beautiful story of endosymbiosis in his book, John Archibald, One Plus One Equals One: Symbiosis and the Origin of Complex Life (Oxford: Oxford University Press, 2014). However, this historical narrative could be treated as synecdochal of how the molecular revolution has changed evolutionary biology forever, and that is how Archibald has structured his book. I will address the encompassing theme of molecular methods in detail, but also pay careful attention to the endosymbiosis thread in its own right.


Endosymbiosis Eukaryote evolution Molecular evolution Organelle evolution 



Many thanks to Peter Godfrey-Smith and Susan Spath for comments on an earlier draft.


  1. Adl SM et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–514CrossRefGoogle Scholar
  2. Archibald J (2014) One plus one equals one: symbiosis and the origin of complex life. Oxford University Press, OxfordGoogle Scholar
  3. Atwood KC, Schmeider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37:146–155CrossRefGoogle Scholar
  4. Birky CW Jr, Mauryama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513–527Google Scholar
  5. Bolte K, Rensing SA, Maier U-G (2014) The evolution of eukaryotic cells from the perspective of peroxisomes. BioEssays 37:195–203CrossRefGoogle Scholar
  6. Booth A, Doolittle WF (2015) Eukaryogenesis: how special really? (forthcoming)Google Scholar
  7. Bourke AFG (2011) Principles of social evolution. Oxford University Press, Oxford UKCrossRefGoogle Scholar
  8. Brock TD (1988) The bacterial nucleus: a history. Microbiol Rev 52:397–411Google Scholar
  9. Brown MW, Kolisko M, Silberman JD, Roger AJ (2012) Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22:1123–1127CrossRefGoogle Scholar
  10. Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, Simpson AGB, Roger AJ (2013) Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc R Soc Lond B 280:20131755CrossRefGoogle Scholar
  11. Burki F, Imanian B, Hehenberger E, Hirakawa Y, Maruyama S, Keeling PJ (2014) Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot Cell 13:246–255CrossRefGoogle Scholar
  12. Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton NJGoogle Scholar
  13. Canfield DE, Poulton SW, Narbonne GM (2007) Late-neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95CrossRefGoogle Scholar
  14. Caron DA (2013) Towards a molecular taxonomy for protists: benefits, risks, and applications in plankton ecology. J Eukaryot Microbiol 60:407–413CrossRefGoogle Scholar
  15. Cavalier-Smith T (1987) The origin of eukaryote and archaebacterial cells. Ann NY Acad Sci 503:17–54CrossRefGoogle Scholar
  16. Cavalier-Smith T (1992) The number of symbiotic origins of organelles. BioSystems 28:91–106CrossRefGoogle Scholar
  17. Clarke E (2011) Plant individuality and multilevel selection theory. In: Calcott B, Sterelny K (eds) Major transitions in evolution revisited. MIT Press, Cambridge MA, pp 227–250CrossRefGoogle Scholar
  18. Cleland CE (2002) Methodological and epistemic differences between historical science and experimental science. Philos Sci 69:474–496CrossRefGoogle Scholar
  19. Costerton JW (1988) Structure and plasticity at various organization levels in the bacterial cell. Can J Microbiol 14:513–521CrossRefGoogle Scholar
  20. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA 105:20356–20361CrossRefGoogle Scholar
  21. Dagan T, Martin W (2009) Getting a better picture of microbial evolution en route to a network of genomes. Philos Trans R Soc Lond B Biol Sci 364:2187–2196CrossRefGoogle Scholar
  22. Davis RH (2003) The microbial models of molecular biology. Oxford University Press, OxfordCrossRefGoogle Scholar
  23. Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life. Proc Natl Acad Sci USA 104:2043–2049CrossRefGoogle Scholar
  24. Eme L, Sharpe SC, Brown MW, Roger AJ (2014) On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb Perspect Biol 6. doi: 10.1101/cshperspect.a06139
  25. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360CrossRefGoogle Scholar
  26. Fenchel T, Perry T, Thane A (1977) Anaerobosis and symbiosis with bacteria in free-living ciliates. J Protozool 24:154–163CrossRefGoogle Scholar
  27. Finlay BJ (2004) Protist taxonomy: an ecological perspective. Philos Trans R Soc Lond B Biol Sci 359:599–610CrossRefGoogle Scholar
  28. Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, OxfordCrossRefGoogle Scholar
  29. Godfrey-Smith P (2013) Darwinian individuals. In: Bouchard F, Huneman P (eds) From groups to individuals: perspectives on biological associations and emerging individuals. MIT Press, Cambridge MA, pp 17–36Google Scholar
  30. Grattepanche J-D, Santoferrara LF, McManus GB, Katz LA (2014) Diversity of diversity: conceptual and methodological differences in biodiversity estimates of eukaryotic microbes as compared to bacteria. Trends Microbiol 22:432–437CrossRefGoogle Scholar
  31. Gray MW (1994) One plus one equals one: the making of a cryptomonad. ASM News 60:423–427Google Scholar
  32. Gray MW (2014) The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6:016097CrossRefGoogle Scholar
  33. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42Google Scholar
  34. Gribaldo S, Poole AM, Daubin V, Forterre P, Brochier-Armanet C (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature Rev Microbiol 8:743–752CrossRefGoogle Scholar
  35. Heiss AA, Walker G, Simpson AGB (2013) The microtubular cytoskeleton of the apusomonad Thecamonas, a sister lineage to the opisthokonts. Protist 164:598–621CrossRefGoogle Scholar
  36. Howe CJ, Barbrook AC, Nisbet RER, Lockhart PJ, Larkum AWD (2008) The origin of plastids. Phil Trans R Soc Lond B 363:2675–2685CrossRefGoogle Scholar
  37. Jacob F, Wollman EL (1961) Sexuality and the genetics of bacteria. Academic Press, NYGoogle Scholar
  38. Jeon KW, Jeon MS (1976) Endosymbiosis in amoebae: recently established endosymbionts have become required cytoplasmic components. J Cell Physiol 89:337–344CrossRefGoogle Scholar
  39. Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Phil Trans R Soc London B 365:729–748CrossRefGoogle Scholar
  40. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607CrossRefGoogle Scholar
  41. Koonin EV (2007) The Biological Big Bang model for the major transitions in evolution. Biol Direct 2:21. doi: 10.1186/1745-6150-2-21 CrossRefGoogle Scholar
  42. Koonin EV (2010) The incredible expanding ancestor of eukaryotes. Cell 140:606–608CrossRefGoogle Scholar
  43. Koonin EV, Yutin N (2014) The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb Perspect Biol 6:a016188CrossRefGoogle Scholar
  44. Koumandou VL, Wickstead B, Ginger ML, van der Giezen M, Dacks JB, Field MC (2013) Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit Rev Biochem Mol Biol 48:373–396CrossRefGoogle Scholar
  45. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934CrossRefGoogle Scholar
  46. Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–196CrossRefGoogle Scholar
  47. Lorch IJ, Jeon KW (1980) Resuscitation of amebae deprived of essential symbiotes: micrurgical studies. J Protozool 27:423–426CrossRefGoogle Scholar
  48. Love AC, Travisano M (2013) Microbes modeling ontogeny. Biol Philos 28:161–188CrossRefGoogle Scholar
  49. Maguire F, Richards TA (2014) Organelle evolution: a mosaic of ‘mitochondrial’ functions. Curr Biol 24:R518–R520CrossRefGoogle Scholar
  50. Mann DG (2000) The species concept in diatoms. Phycologia 38:437–495CrossRefGoogle Scholar
  51. Margulis L (1975) The microbes’ contribution to evolution. BioSystems 7:266–292CrossRefGoogle Scholar
  52. Margulis L (1996) Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci USA 93:1071–1076CrossRefGoogle Scholar
  53. Margulis L (2004) Serial endosymbiotic theory (SET) and composite individuality: transition from bacterial to eukaryotic genomes. Microbiol Today 31:172–174Google Scholar
  54. Margulis L, Chapman M, Guerrero R, Hall J (2006) The last eukaryotic common ancestor (LECA): acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic eon. Proc Natl Acad Sci USA 103:13080–13085CrossRefGoogle Scholar
  55. Martijn J, Ettema TJG (2013) From archaeon to eukaryote: the evolutionary dark ages of the cell. Biochem Soc Trans 41:451–457CrossRefGoogle Scholar
  56. Maynard Smith J, Szathmáry E (1997) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  57. Michod RE (2005) On the transfer of fitness from the cell to the multicellular organism. Biol Philos 20:967–987CrossRefGoogle Scholar
  58. Moran N (2014) The complexity chronicles. Nature 510:338–339CrossRefGoogle Scholar
  59. Müller M et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495CrossRefGoogle Scholar
  60. Nowack ECM (2014) Paulinella chromatophora—rethinking the transition from endosymbiont to organelle. Acta Soc Bot Pol 83:387–397CrossRefGoogle Scholar
  61. Nowack ECM, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA 109:5340–5345CrossRefGoogle Scholar
  62. O’Malley MA (2010) The first eukaryote cell: an unfinished history of contestation. Stud Hist Philos Biol Biomed Sci 41:212–224CrossRefGoogle Scholar
  63. O’Malley MA, Powell R. Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution (forthcoming)Google Scholar
  64. O’Malley MA, Velicer GJ, Travisano M, Bolker JA (2015) How do microbial populations and communities function as model systems? (forthcoming)Google Scholar
  65. Philippe H et al (2000) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc R Soc Lond B 267:1213–1221CrossRefGoogle Scholar
  66. Pradeu T (2013) Immunity and the emergence of individuality. In: Bouchard F, Huneman P (eds) From groups to individuals: evolution and emerging individuality. MIT Press, Cambridge MA, pp 77–97Google Scholar
  67. Race HL, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends Genet 15:364–370CrossRefGoogle Scholar
  68. Rainey PB, Rainey K (2003) Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72–74CrossRefGoogle Scholar
  69. Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109:1595–1600CrossRefGoogle Scholar
  70. Ruiz-Trillo I (2014) How animals emerged? A genomics and cell biology perspective. Protist 2014, Banff (Canada), August 3–8,
  71. Sober E, Wilson DS (1994) A critical review of philosophical work on the units of selection problem. Philos Sci 61:534–555CrossRefGoogle Scholar
  72. Spath S (2015) Review of ‘One Plus One Equals One’. NCSE Reports (forthcoming)Google Scholar
  73. Stairs CW et al (2014) A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia. Curr Biol 24:1176–1186CrossRefGoogle Scholar
  74. Taylor FJR (1974) II: Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23:229–258CrossRefGoogle Scholar
  75. Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16:R1016–R1017CrossRefGoogle Scholar
  76. Turner D (2005) Local underdetermination in historical science. Philos Sci 72:209–230CrossRefGoogle Scholar
  77. van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56:221–231CrossRefGoogle Scholar
  78. Williams TA (2014) Evolution: rooting the eukaryotic tree of life. Curr Biol 24:R151–R152CrossRefGoogle Scholar
  79. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090CrossRefGoogle Scholar
  80. Wolf YI, Koonin EV (2013) Genome reduction as the dominant mode of evolution. BioEssays 35:829–837CrossRefGoogle Scholar
  81. Woolfit M, Bromham L (2003) Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol 20:1545–1555CrossRefGoogle Scholar
  82. Yabuki A et al (2014) Palpitomonas bilix represtents a basal cryptist lineage: insight into the character evolution in Cryptista. Sci Rep 4:464. doi: 10.1038/srep04641 CrossRefGoogle Scholar
  83. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of PhilosophyUniversity of SydneySydneyAustralia

Personalised recommendations