Abstract
All complex life is composed of eukaryotic (nucleated) cells. The eukaryotic cell arose from prokaryotes just once in four billion years, and otherwise prokaryotes show no tendency to evolve greater complexity. Why not? Prokaryotic genome size is constrained by bioenergetics. The endosymbiosis that gave rise to mitochondria restructured the distribution of DNA in relation to bioenergetic membranes, permitting a remarkable 200,000-fold expansion in the number of genes expressed. This vast leap in genomic capacity was strictly dependent on mitochondrial power, and prerequisite to eukaryote complexity: the key innovation en route to multicellular life.
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References
Rokas, A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235–251 (2008)
Lindsay, M. R. et al. Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175, 413–429 (2001)
Smith, J. M., Smith, N. H., O’Rourke, M. & Spratt, B. G. How clonal are bacteria? Proc. Natl Acad. Sci. USA 90, 4384–4388 (1993)
Bentley, S. D. et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147 (2002)
Pinevich, A. V. Intracytoplasmic membrane structures in bacteria. Endocyt. Cell Res. 12, 9–40 (1997)
Robinson, N. P. & Bell, S. D. Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes. Proc. Natl Acad. Sci. USA 104, 5806–5811 (2007)
Schulz, H. N. & Jorgensen, B. B. Big bacteria. Annu. Rev. Microbiol. 55, 105–137 (2001)
Mendell, J. E., Clements, K. D., Choat, J. H. & Angert, E. R. Extreme polyploidy in a large bacterium. Proc. Natl Acad. Sci. USA 105, 6730–6734 (2008)
Vats, P., Yu, J. & Rothfield, L. The dynamic nature of the bacterial cytoskeleton. Cell. Mol. Life Sci. 66, 3353–3362 (2009)
Davidov, Y. & Jurkevitch, E. Predation between prokaryotes and the origin of eukaryotes. Bioessays 31, 748–757 (2009)
Moran, N. A. Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl Acad. Sci. USA 104, 8627–8633 (2007)
Simon, D. M. & Zimmerly, S. A diversity of uncharacterized retroelements in bacteria. Nucleic Acids Res. 36, 7219–7229 (2008)
Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005)
Lonhienne, T. G. A. et al. Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus . Proc. Natl Acad. Sci. USA 107, 12883–12888 (2010)
von Dohlen, C. D., Kohler, S., Alsop, S. T. & McManus, W. R. Mealybug β-proteobacterial symbionts contain γ-proteobacterial symbionts. Nature 412, 433–436 (2001)A rare example of a prokaryote residing as an endosymbiont within a prokaryotic host, demonstrating that phagocytosis is not prerequisite to endosymbiosis.
Wujek, D. E. Intracellular bacteria in the blue-green-alga Pleurocapsa minor . Trans. Am. Microsc. Soc. 98, 143–145 (1979)
Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 1401–1404 (2003)
Smith, J. M. & Szathmary, E. The Major Transitions in Evolution (Oxford Univ.Press, 1995)
Cavalier-Smith, T. Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307–322 (2009)
de Duve, C. The origin of eukaryotes: a reappraisal. Nature Rev. Genet. 8, 395–403 (2007)
Rivera, M. C. & Lake, J. A. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155 (2004)
Koonin, E. V. Darwinian evolution in the light of genomics. Nucleic Acids Res. 37, 1011–1034 (2009)
Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimeric origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760 (2007)
Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20356–20361 (2008)An important contribution, using a state of the art phylogenetic repertoire, to show that the host that acquired the mitochondrion was an archaebacterium (a prokaryote).
Tovar, J. et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172–176 (2003)
van der Giezen, M. Hydrogenosomes and mitosomes: conservation and evolution of functions. J. Eukaryot. Microbiol. 56, 221–231 (2009)
Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998)
Tielens, A. G. M. et al. Mitochondria as we don’t know them. Trends Biochem. Sci. 27, 564–572 (2002)
Harold, F. M. The Vital Force: A Study of Bioenergetics (Freeman, 1986)
Walker, J. C., Margulis, L. & Rambler, M. Reassessment of roles of oxygen and ultraviolet light in Precambrian evolution. Nature 264, 620–624 (1976)
Johnston, D. T., Wolfe-Simon, F., Pearson, A. & Knoll, A. H. Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age. Proc. Natl Acad. Sci. USA 106, 16925–16929 (2009)
Makarieva, A. M., Gorshkov, V. G. & Li, B. L. Energetics of the smallest: do bacteria breathe at the same rate as whales? Proc. R. Soc. Lond. B 272, 2219–2224 (2005)
Fenchel, T. & Finlay, B. J. Respiration rates in heterotrophic, free-living protozoa. Microb. Ecol. 9, 99–122 (1983)
Vellai, T. & Vida, G. The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells. Proc. R. Soc. Lond. B 266, 1571–1577 (1999)
Wagner, A. Energy constraints on the evolution of gene expression. Mol. Biol. Evol. 22, 1365–1374 (2005)
Nilsson, M., Bülow, L. & Wahlund, K. Use of flow field-flow fractionation for the rapid quantitation of ribosome and ribosomal subunits in Escherichia coli at different protein production conditions. Biotechnol. Bioeng. 54, 461–467 (1997)
Weibel, E. R. et al. Correlated morphometric and biochemical studies of the liver cell. J. Cell Biol. 42, 68–91 (1969)
Gray, M. W., Lang, B. F. & Burger, G. Mitochondria of protists. Annu. Rev. Genet. 38, 477–524 (2004)
Daniels, E. W. & Breyer, E. P. Starvation effects on the ultrastructure of amoeba mitochondria. Z. Zellforsch. 91, 159–169 (1968)
Aury, J.-M. et al. Global trends of whole genome duplications revealed by the ciliate Paramecium tetraurelia . Nature 444, 171–178 (2006)
Lane, N. Power, Sex, Suicide: Mitochondria and the Meaning of Life (Oxford Univ. Press, 2005)
Koonin, E. V. et al. A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol. 5, R7 (2004)A seminal contribution that underscores the uniqueness of eukaryotic genomes with respect to their enriched protein content relative to prokaryotic forebears.
Fritz-Laylin, L. K. et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642 (2010)
Kunin, V. & Ouzounis, C. A. The balance of driving forces during genome evolution in prokaryotes. Genome Res. 13, 1589–1594 (2003)
Kuo, C. H. & Ochman, H. The extinction dynamics of bacterial pseudogenes. PLoS Genet. 6, e1001050 (2010)
Vellai, T., Takacs, K. & Vida, G. A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 46, 499–507 (1998)
Brocchieri, L. & Karlin, S. Protein length in eukaryotic and prokaryotic proteomes. Nucleic Acids Res. 33, 3390–3400 (2005)
Peterson, K. J., Dietrich, M. R. & McPeek, M. A. MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion. Bioessays 31, 736–747 (2009)
Bidle, K. D. & Falkowski, P. G. Cell death in planktonic, photosynthetic microorganisms. Nature Rev. Microbiol. 2, 643–655 (2004)
Allen, J. F. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165, 609–631 (1993)
Allen, J. F. The function of genomes in bioenergetic organelles. Philos. Trans. R. Soc. Lond. B 358, 19–38 (2003)Presents compelling bioenergetic reasons, necessary and sufficient, to account for the retention of genes involved in membrane-associated electron transport in mitochondria (and chloroplasts).
Williams, R. S. Mitochondrial gene expression in mammalian striated muscle: evidence that variation in gene dosage is the major regulatory event. J. Biol. Chem. 261, 12390–12394 (1986)
Williams, R. S. et al. Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. J. Biol. Chem. 261, 376–380 (1986)
Shay, J. W., Pierce, D. J. & Werbin, H. Mitochondrial DNA copy number is proportional to total cell DNA under a variety of growth conditions. J. Biol. Chem. 265, 14802–14807 (1990)
Schapira, A. H. Mitochondrial disease. Lancet 368, 70–82 (2006)
Rocher, C. et al. Influence of mitochondrial DNA level on cellular energy metabolism: implications for mitochondrial diseases. J. Bioenerg. Biomembr. 40, 59–67 (2008)A systematic study demonstrating the linear dependence of metabolic rate on mtDNA copy number.
Moreno-Loshuertos, R. et al. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nature Genet. 38, 1261–1268 (2006)An important paper showing that free-radical signals modulate mtDNA copy number and the rate of ATP synthesis.
Bai, Y., Shakeley, R. M. & Attardi, G. Tight control of respiration by NADH dehydrogenase ND5 subunit gene expression in mouse mitochondria. Mol. Cell. Biol. 20, 805–815 (2000)A seminal contribution, showing that the rate of transcription of a mtDNA-encoded respiratory subunit controls the overall rate of respiration.
Chomyn, A. Mitochondrial genetic control of assembly and function of complex I in mammalian cells. J. Bioenerg. Biomembr. 33, 251–257 (2001)
Piruat, J. I. & López-Barneo, J. Oxygen tension regulates mitochondrial DNA-encoded complex I gene expression. J. Biol. Chem. 280, 42676–42684 (2005)
Shimizu, M. et al. Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc. Natl Acad. Sci. USA 107, 10760–10764 (2010)
Schulz, H. N. The genus Thiomargarita . Prokaryotes 6, 1156–1163 (2006)
Timmis, J. N. et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5, 123–135 (2004)
Lane, C. E. & Archibald, J. M. The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol. Evol. 23, 268–275 (2008)
Ebersbach, G. & Gerdes, K. Plasmid segregation mechanisms. Annu. Rev. Genet. 39, 453–479 (2005)
Yang, S., Doolittle, R. F. & Bourne, P. E. Phylogeny determined by protein domain content. Proc. Natl Acad. Sci. USA 102, 373–378 (2005)
Lane, N. Life Ascending: The Ten Great Inventions of Evolution (Norton, 2009)
Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009)
Brighouse, A., Dacks, J. B. & Field, M. C. Rab protein evolution and the history of the eukaryotic endomembrane system. Cell. Mol. Life Sci. 67, 3449–3465 (2010)
Martin, W. & Koonin, E. V. Introns and the origin of nucleus–cytosol compartmentalization. Nature 440, 41–45 (2006)
Forterre, P. & Gribaldo, S. Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc. Natl Acad. Sci. USA 107, 12739–12740 (2010)
Kurland, C. G., Collins, L. J. & Penny, D. Genomics and the irreducible nature of eukaryote cells. Science 312, 1011–1014 (2006)
Schulz, H. N. & de Beer, D. Uptake rates of oxygen and sulphide measured with individual Thiomargarita namibiensis cells by using microelectrodes. Appl. Environ. Microbiol. 68, 5746–5749 (2002)
Parfrey, L. W., Lahr, D. J. G. & Katz, L. A. The dynamic nature of eukaryotic genomes. Mol. Biol. Evol. 25, 787–794 (2008)
Acknowledgements
We are indebted to A. Hidalgo, D. Braben, F. Harold, J. Ellis, H. Schulz-Vogt, J. Allen, G. Shields and L. Sweetlove for many discussions and comments on the manuscript, M. Farmer, H. Schulz-Vogt and R. Allen for microscopic images. N.L. is very grateful to the UCL Provost’s Venture Research Fellowship, W.M. to the German Research Foundation and the European Research Council (Networkorigins) for funding.
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Lane, N., Martin, W. The energetics of genome complexity. Nature 467, 929–934 (2010). https://doi.org/10.1038/nature09486
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DOI: https://doi.org/10.1038/nature09486
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