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.
Notes
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.
The peroxisome may possibly owe its existence to the mitochondrion (Bolte et al. 2014) but not to a new incoming endosymbiont.
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
Adl SM et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–514
Archibald J (2014) One plus one equals one: symbiosis and the origin of complex life. Oxford University Press, Oxford
Atwood KC, Schmeider LK, Ryan FJ (1951) Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 37:146–155
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
Bolte K, Rensing SA, Maier U-G (2014) The evolution of eukaryotic cells from the perspective of peroxisomes. BioEssays 37:195–203
Booth A, Doolittle WF (2015) Eukaryogenesis: how special really? (forthcoming)
Bourke AFG (2011) Principles of social evolution. Oxford University Press, Oxford UK
Brock TD (1988) The bacterial nucleus: a history. Microbiol Rev 52:397–411
Brown MW, Kolisko M, Silberman JD, Roger AJ (2012) Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22:1123–1127
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
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
Buss LW (1987) The evolution of individuality. Princeton University Press, Princeton NJ
Canfield DE, Poulton SW, Narbonne GM (2007) Late-neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95
Caron DA (2013) Towards a molecular taxonomy for protists: benefits, risks, and applications in plankton ecology. J Eukaryot Microbiol 60:407–413
Cavalier-Smith T (1987) The origin of eukaryote and archaebacterial cells. Ann NY Acad Sci 503:17–54
Cavalier-Smith T (1992) The number of symbiotic origins of organelles. BioSystems 28:91–106
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
Cleland CE (2002) Methodological and epistemic differences between historical science and experimental science. Philos Sci 69:474–496
Costerton JW (1988) Structure and plasticity at various organization levels in the bacterial cell. Can J Microbiol 14:513–521
Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM (2008) The archaebacterial origin of eukaryotes. Proc Natl Acad Sci USA 105:20356–20361
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
Davis RH (2003) The microbial models of molecular biology. Oxford University Press, Oxford
Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life. Proc Natl Acad Sci USA 104:2043–2049
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
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
Fenchel T, Perry T, Thane A (1977) Anaerobosis and symbiosis with bacteria in free-living ciliates. J Protozool 24:154–163
Finlay BJ (2004) Protist taxonomy: an ecological perspective. Philos Trans R Soc Lond B Biol Sci 359:599–610
Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, Oxford
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
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
Gray MW (1994) One plus one equals one: the making of a cryptomonad. ASM News 60:423–427
Gray MW (2014) The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb Perspect Biol 6:016097
Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Microbiol Rev 46:1–42
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
Heiss AA, Walker G, Simpson AGB (2013) The microtubular cytoskeleton of the apusomonad Thecamonas, a sister lineage to the opisthokonts. Protist 164:598–621
Howe CJ, Barbrook AC, Nisbet RER, Lockhart PJ, Larkum AWD (2008) The origin of plastids. Phil Trans R Soc Lond B 363:2675–2685
Jacob F, Wollman EL (1961) Sexuality and the genetics of bacteria. Academic Press, NY
Jeon KW, Jeon MS (1976) Endosymbiosis in amoebae: recently established endosymbionts have become required cytoplasmic components. J Cell Physiol 89:337–344
Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Phil Trans R Soc London B 365:729–748
Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607
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
Koonin EV (2010) The incredible expanding ancestor of eukaryotes. Cell 140:606–608
Koonin EV, Yutin N (2014) The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb Perspect Biol 6:a016188
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
Lane N, Martin W (2010) The energetics of genome complexity. Nature 467:929–934
Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–196
Lorch IJ, Jeon KW (1980) Resuscitation of amebae deprived of essential symbiotes: micrurgical studies. J Protozool 27:423–426
Love AC, Travisano M (2013) Microbes modeling ontogeny. Biol Philos 28:161–188
Maguire F, Richards TA (2014) Organelle evolution: a mosaic of ‘mitochondrial’ functions. Curr Biol 24:R518–R520
Mann DG (2000) The species concept in diatoms. Phycologia 38:437–495
Margulis L (1975) The microbes’ contribution to evolution. BioSystems 7:266–292
Margulis L (1996) Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci USA 93:1071–1076
Margulis L (2004) Serial endosymbiotic theory (SET) and composite individuality: transition from bacterial to eukaryotic genomes. Microbiol Today 31:172–174
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
Martijn J, Ettema TJG (2013) From archaeon to eukaryote: the evolutionary dark ages of the cell. Biochem Soc Trans 41:451–457
Maynard Smith J, Szathmáry E (1997) The major transitions in evolution. Oxford University Press, Oxford
Michod RE (2005) On the transfer of fitness from the cell to the multicellular organism. Biol Philos 20:967–987
Moran N (2014) The complexity chronicles. Nature 510:338–339
Müller M et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495
Nowack ECM (2014) Paulinella chromatophora—rethinking the transition from endosymbiont to organelle. Acta Soc Bot Pol 83:387–397
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
O’Malley MA (2010) The first eukaryote cell: an unfinished history of contestation. Stud Hist Philos Biol Biomed Sci 41:212–224
O’Malley MA, Powell R. Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution (forthcoming)
O’Malley MA, Velicer GJ, Travisano M, Bolker JA (2015) How do microbial populations and communities function as model systems? (forthcoming)
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
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
Race HL, Herrmann RG, Martin W (1999) Why have organelles retained genomes? Trends Genet 15:364–370
Rainey PB, Rainey K (2003) Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72–74
Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109:1595–1600
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
Sober E, Wilson DS (1994) A critical review of philosophical work on the units of selection problem. Philos Sci 61:534–555
Spath S (2015) Review of ‘One Plus One Equals One’. NCSE Reports (forthcoming)
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
Taylor FJR (1974) II: Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 23:229–258
Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol 16:R1016–R1017
Turner D (2005) Local underdetermination in historical science. Philos Sci 72:209–230
van der Giezen M (2009) Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 56:221–231
Williams TA (2014) Evolution: rooting the eukaryotic tree of life. Curr Biol 24:R151–R152
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090
Wolf YI, Koonin EV (2013) Genome reduction as the dominant mode of evolution. BioEssays 35:829–837
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
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
Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48
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Many thanks to Peter Godfrey-Smith and Susan Spath for comments on an earlier draft.
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O’Malley, M.A. Molecular organisms. Biol Philos 31, 571–589 (2016). https://doi.org/10.1007/s10539-015-9482-2
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DOI: https://doi.org/10.1007/s10539-015-9482-2