Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Molecular organisms

John Archibald, One Plus One Equals One: Symbiosis and the Origin of Complex Life. Oxford: Oxford University Press, 2014

  • 801 Accesses

Abstract

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.

This is a preview of subscription content, log in to check access.

Fig. 1

Notes

  1. 1.

    All images from Wikimedia Commons: (1) Rhizobia nodules by Dave Whitaker; (2) Life cycle of retrovirus by Mrdavis21; (3) Wolbachia in insect cell by Scott O’Neill; (4) Buchnera in pea aphid bacteriocyte by J. White and N. Moran; (5a) Mitochondrion by Nevit; (5b) Chloroplasts in Mnium stellare by Thomas Geier.

  2. 2.

    The peroxisome may possibly owe its existence to the mitochondrion (Bolte et al. 2014) but not to a new incoming endosymbiont.

  3. 3.

    I have seen philosophical publications with all three of these organelles asserted as endosymbiotic in origin, but there is no need to name those papers here. Seeing Margulis as the main source of information for the endosymbiosis of organelles may be the cause of such excesses—simply because of her exuberance in asserting symbioses as the most important and ubiquitous evolutionary cause.

References

  1. Adl SM et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–514

  2. Archibald J (2014) One plus one equals one: symbiosis and the origin of complex life. Oxford University Press, Oxford

  3. Atwood KC, Schmeider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37:146–155

  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 103:513–527

  5. Bolte K, Rensing SA, Maier U-G (2014) The evolution of eukaryotic cells from the perspective of peroxisomes. BioEssays 37:195–203

  6. Booth A, Doolittle WF (2015) Eukaryogenesis: how special really? (forthcoming)

  7. Bourke AFG (2011) Principles of social evolution. Oxford University Press, Oxford UK

  8. Brock TD (1988) The bacterial nucleus: a history. Microbiol Rev 52:397–411

  9. Brown MW, Kolisko M, Silberman JD, Roger AJ (2012) Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22:1123–1127

  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 280:20131755

  11. Burki F, Imanian B, Hehenberger E, Hirakawa Y, Maruyama S, Keeling PJ (2014) Endosymbiotic gene transfer in tertiary plastid-containing dinoflagellates. Eukaryot Cell 13:246–255

  12. Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton NJ

  13. Canfield DE, Poulton SW, Narbonne GM (2007) Late-neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95

  14. Caron DA (2013) Towards a molecular taxonomy for protists: benefits, risks, and applications in plankton ecology. J Eukaryot Microbiol 60:407–413

  15. Cavalier-Smith T (1987) The origin of eukaryote and archaebacterial cells. Ann NY Acad Sci 503:17–54

  16. Cavalier-Smith T (1992) The number of symbiotic origins of organelles. BioSystems 28:91–106

  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 227–250

  18. Cleland CE (2002) Methodological and epistemic differences between historical science and experimental science. Philos Sci 69:474–496

  19. Costerton JW (1988) Structure and plasticity at various organization levels in the bacterial cell. Can J Microbiol 14:513–521

  20. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA 105:20356–20361

  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 364:2187–2196

  22. Davis RH (2003) The microbial models of molecular biology. Oxford University Press, Oxford

  23. Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life. Proc Natl Acad Sci USA 104:2043–2049

  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 305:354–360

  26. Fenchel T, Perry T, Thane A (1977) Anaerobosis and symbiosis with bacteria in free-living ciliates. J Protozool 24:154–163

  27. Finlay BJ (2004) Protist taxonomy: an ecological perspective. Philos Trans R Soc Lond B Biol Sci 359:599–610

  28. Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, Oxford

  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 17–36

  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 22:432–437

  31. Gray MW (1994) One plus one equals one: the making of a cryptomonad. ASM News 60:423–427

  32. Gray MW (2014) The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6:016097

  33. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42

  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 8:743–752

  35. Heiss AA, Walker G, Simpson AGB (2013) The microtubular cytoskeleton of the apusomonad Thecamonas, a sister lineage to the opisthokonts. Protist 164:598–621

  36. Howe CJ, Barbrook AC, Nisbet RER, Lockhart PJ, Larkum AWD (2008) The origin of plastids. Phil Trans R Soc Lond B 363:2675–2685

  37. Jacob F, Wollman EL (1961) Sexuality and the genetics of bacteria. Academic Press, NY

  38. Jeon KW, Jeon MS (1976) Endosymbiosis in amoebae: recently established endosymbionts have become required cytoplasmic components. J Cell Physiol 89:337–344

  39. Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Phil Trans R Soc London B 365:729–748

  40. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607

  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

  42. Koonin EV (2010) The incredible expanding ancestor of eukaryotes. Cell 140:606–608

  43. Koonin EV, Yutin N (2014) The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb Perspect Biol 6:a016188

  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 48:373–396

  45. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934

  46. Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–196

  47. Lorch IJ, Jeon KW (1980) Resuscitation of amebae deprived of essential symbiotes: micrurgical studies. J Protozool 27:423–426

  48. Love AC, Travisano M (2013) Microbes modeling ontogeny. Biol Philos 28:161–188

  49. Maguire F, Richards TA (2014) Organelle evolution: a mosaic of ‘mitochondrial’ functions. Curr Biol 24:R518–R520

  50. Mann DG (2000) The species concept in diatoms. Phycologia 38:437–495

  51. Margulis L (1975) The microbes’ contribution to evolution. BioSystems 7:266–292

  52. Margulis L (1996) Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci USA 93:1071–1076

  53. Margulis L (2004) Serial endosymbiotic theory (SET) and composite individuality: transition from bacterial to eukaryotic genomes. Microbiol Today 31:172–174

  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 103:13080–13085

  55. Martijn J, Ettema TJG (2013) From archaeon to eukaryote: the evolutionary dark ages of the cell. Biochem Soc Trans 41:451–457

  56. Maynard Smith J, Szathmáry E (1997) The major transitions in evolution. Oxford University Press, Oxford

  57. Michod RE (2005) On the transfer of fitness from the cell to the multicellular organism. Biol Philos 20:967–987

  58. Moran N (2014) The complexity chronicles. Nature 510:338–339

  59. Müller M et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495

  60. Nowack ECM (2014) Paulinella chromatophora—rethinking the transition from endosymbiont to organelle. Acta Soc Bot Pol 83:387–397

  61. Nowack ECM, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci USA 109:5340–5345

  62. O’Malley MA (2010) The first eukaryote cell: an unfinished history of contestation. Stud Hist Philos Biol Biomed Sci 41:212–224

  63. O’Malley MA, Powell R. Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution (forthcoming)

  64. O’Malley MA, Velicer GJ, Travisano M, Bolker JA (2015) How do microbial populations and communities function as model systems? (forthcoming)

  65. Philippe H et al (2000) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc R Soc Lond B 267:1213–1221

  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 77–97

  67. Race HL, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends Genet 15:364–370

  68. Rainey PB, Rainey K (2003) Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72–74

  69. Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109:1595–1600

  70. Ruiz-Trillo I (2014) How animals emerged? A genomics and cell biology perspective. Protist 2014, Banff (Canada), August 3–8, http://www.ualberta.ca/~cklinger/Protist2014/ConfInfo.html

  71. Sober E, Wilson DS (1994) A critical review of philosophical work on the units of selection problem. Philos Sci 61:534–555

  72. Spath S (2015) Review of ‘One Plus One Equals One’. NCSE Reports (forthcoming)

  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 24:1176–1186

  74. Taylor FJR (1974) II: Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23:229–258

  75. Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16:R1016–R1017

  76. Turner D (2005) Local underdetermination in historical science. Philos Sci 72:209–230

  77. van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56:221–231

  78. Williams TA (2014) Evolution: rooting the eukaryotic tree of life. Curr Biol 24:R151–R152

  79. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

  80. Wolf YI, Koonin EV (2013) Genome reduction as the dominant mode of evolution. BioEssays 35:829–837

  81. Woolfit M, Bromham L (2003) Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes. Mol Biol Evol 20:1545–1555

  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

  83. Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48

Download references

Acknowledgments

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

Author information

Correspondence to Maureen A. O’Malley.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

O’Malley, M.A. Molecular organisms. Biol Philos 31, 571–589 (2016). https://doi.org/10.1007/s10539-015-9482-2

Download citation

Keywords

  • Endosymbiosis
  • Eukaryote evolution
  • Molecular evolution
  • Organelle evolution