Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The energetics of genome complexity

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Cell complexity, cell simplicity and energy supply for both.
Figure 2: The cellular power struggle.

Similar content being viewed by others

References

  1. Rokas, A. The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu. Rev. Genet. 42, 235–251 (2008)

    Article  CAS  PubMed  Google Scholar 

  2. Lindsay, M. R. et al. Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175, 413–429 (2001)

    Article  CAS  PubMed  Google Scholar 

  3. 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)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bentley, S. D. et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147 (2002)

    Article  ADS  PubMed  Google Scholar 

  5. Pinevich, A. V. Intracytoplasmic membrane structures in bacteria. Endocyt. Cell Res. 12, 9–40 (1997)

    Google Scholar 

  6. 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)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Schulz, H. N. & Jorgensen, B. B. Big bacteria. Annu. Rev. Microbiol. 55, 105–137 (2001)

    Article  CAS  PubMed  Google Scholar 

  8. 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)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Vats, P., Yu, J. & Rothfield, L. The dynamic nature of the bacterial cytoskeleton. Cell. Mol. Life Sci. 66, 3353–3362 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Davidov, Y. & Jurkevitch, E. Predation between prokaryotes and the origin of eukaryotes. Bioessays 31, 748–757 (2009)

    Article  CAS  PubMed  Google Scholar 

  11. Moran, N. A. Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl Acad. Sci. USA 104, 8627–8633 (2007)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Simon, D. M. & Zimmerly, S. A diversity of uncharacterized retroelements in bacteria. Nucleic Acids Res. 36, 7219–7229 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Waters, C. M. & Bassler, B. L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005)

    Article  CAS  PubMed  Google Scholar 

  14. Lonhienne, T. G. A. et al. Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus . Proc. Natl Acad. Sci. USA 107, 12883–12888 (2010)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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.

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Wujek, D. E. Intracellular bacteria in the blue-green-alga Pleurocapsa minor . Trans. Am. Microsc. Soc. 98, 143–145 (1979)

    Article  Google Scholar 

  17. Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 1401–1404 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Smith, J. M. & Szathmary, E. The Major Transitions in Evolution (Oxford Univ.Press, 1995)

    Google Scholar 

  19. Cavalier-Smith, T. Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307–322 (2009)

    Article  CAS  PubMed  Google Scholar 

  20. de Duve, C. The origin of eukaryotes: a reappraisal. Nature Rev. Genet. 8, 395–403 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. Rivera, M. C. & Lake, J. A. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152–155 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Koonin, E. V. Darwinian evolution in the light of genomics. Nucleic Acids Res. 37, 1011–1034 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pisani, D., Cotton, J. A. & McInerney, J. O. Supertrees disentangle the chimeric origin of eukaryotic genomes. Mol. Biol. Evol. 24, 1752–1760 (2007)

    Article  CAS  PubMed  Google Scholar 

  24. 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).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tovar, J. et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172–176 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  27. Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Tielens, A. G. M. et al. Mitochondria as we don’t know them. Trends Biochem. Sci. 27, 564–572 (2002)

    Article  CAS  PubMed  Google Scholar 

  29. Harold, F. M. The Vital Force: A Study of Bioenergetics (Freeman, 1986)

    Google Scholar 

  30. Walker, J. C., Margulis, L. & Rambler, M. Reassessment of roles of oxygen and ultraviolet light in Precambrian evolution. Nature 264, 620–624 (1976)

    Article  ADS  Google Scholar 

  31. 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)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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)

    Article  Google Scholar 

  33. Fenchel, T. & Finlay, B. J. Respiration rates in heterotrophic, free-living protozoa. Microb. Ecol. 9, 99–122 (1983)

    Article  CAS  PubMed  Google Scholar 

  34. Vellai, T. & Vida, G. The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells. Proc. R. Soc. Lond. B 266, 1571–1577 (1999)

    Article  CAS  Google Scholar 

  35. Wagner, A. Energy constraints on the evolution of gene expression. Mol. Biol. Evol. 22, 1365–1374 (2005)

    Article  CAS  PubMed  Google Scholar 

  36. 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)

    Article  CAS  PubMed  Google Scholar 

  37. Weibel, E. R. et al. Correlated morphometric and biochemical studies of the liver cell. J. Cell Biol. 42, 68–91 (1969)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gray, M. W., Lang, B. F. & Burger, G. Mitochondria of protists. Annu. Rev. Genet. 38, 477–524 (2004)

    Article  CAS  PubMed  Google Scholar 

  39. Daniels, E. W. & Breyer, E. P. Starvation effects on the ultrastructure of amoeba mitochondria. Z. Zellforsch. 91, 159–169 (1968)

    Article  CAS  PubMed  Google Scholar 

  40. Aury, J.-M. et al. Global trends of whole genome duplications revealed by the ciliate Paramecium tetraurelia . Nature 444, 171–178 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  41. Lane, N. Power, Sex, Suicide: Mitochondria and the Meaning of Life (Oxford Univ. Press, 2005)

    Google Scholar 

  42. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Fritz-Laylin, L. K. et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642 (2010)

    Article  CAS  PubMed  Google Scholar 

  44. Kunin, V. & Ouzounis, C. A. The balance of driving forces during genome evolution in prokaryotes. Genome Res. 13, 1589–1594 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kuo, C. H. & Ochman, H. The extinction dynamics of bacterial pseudogenes. PLoS Genet. 6, e1001050 (2010)

    Article  PubMed  PubMed Central  Google Scholar 

  46. Vellai, T., Takacs, K. & Vida, G. A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 46, 499–507 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Brocchieri, L. & Karlin, S. Protein length in eukaryotic and prokaryotic proteomes. Nucleic Acids Res. 33, 3390–3400 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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)

    Article  CAS  PubMed  Google Scholar 

  49. Bidle, K. D. & Falkowski, P. G. Cell death in planktonic, photosynthetic microorganisms. Nature Rev. Microbiol. 2, 643–655 (2004)

    Article  CAS  Google Scholar 

  50. 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)

    Article  CAS  PubMed  Google Scholar 

  51. 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).

    Article  CAS  Google Scholar 

  52. 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)

    CAS  PubMed  Google Scholar 

  53. 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)

    CAS  PubMed  Google Scholar 

  54. 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)

    CAS  PubMed  Google Scholar 

  55. Schapira, A. H. Mitochondrial disease. Lancet 368, 70–82 (2006)

    Article  CAS  PubMed  Google Scholar 

  56. 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.

    Article  CAS  PubMed  Google Scholar 

  57. 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.

    Article  CAS  PubMed  Google Scholar 

  58. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chomyn, A. Mitochondrial genetic control of assembly and function of complex I in mammalian cells. J. Bioenerg. Biomembr. 33, 251–257 (2001)

    Article  CAS  PubMed  Google Scholar 

  60. Piruat, J. I. & López-Barneo, J. Oxygen tension regulates mitochondrial DNA-encoded complex I gene expression. J. Biol. Chem. 280, 42676–42684 (2005)

    Article  CAS  PubMed  Google Scholar 

  61. Shimizu, M. et al. Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc. Natl Acad. Sci. USA 107, 10760–10764 (2010)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  62. Schulz, H. N. The genus Thiomargarita . Prokaryotes 6, 1156–1163 (2006)

    Article  Google Scholar 

  63. Timmis, J. N. et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5, 123–135 (2004)

    Article  CAS  PubMed  Google Scholar 

  64. Lane, C. E. & Archibald, J. M. The eukaryotic tree of life: endosymbiosis takes its TOL. Trends Ecol. Evol. 23, 268–275 (2008)

    Article  PubMed  Google Scholar 

  65. Ebersbach, G. & Gerdes, K. Plasmid segregation mechanisms. Annu. Rev. Genet. 39, 453–479 (2005)

    Article  CAS  PubMed  Google Scholar 

  66. Yang, S., Doolittle, R. F. & Bourne, P. E. Phylogeny determined by protein domain content. Proc. Natl Acad. Sci. USA 102, 373–378 (2005)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  67. Lane, N. Life Ascending: The Ten Great Inventions of Evolution (Norton, 2009)

    Google Scholar 

  68. Yutin, N., Wolf, M. Y., Wolf, Y. I. & Koonin, E. V. The origins of phagocytosis and eukaryogenesis. Biol. Direct 4, 9 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  69. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Martin, W. & Koonin, E. V. Introns and the origin of nucleus–cytosol compartmentalization. Nature 440, 41–45 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  71. Forterre, P. & Gribaldo, S. Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc. Natl Acad. Sci. USA 107, 12739–12740 (2010)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kurland, C. G., Collins, L. J. & Penny, D. Genomics and the irreducible nature of eukaryote cells. Science 312, 1011–1014 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  73. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Parfrey, L. W., Lahr, D. J. G. & Katz, L. A. The dynamic nature of eukaryotic genomes. Mol. Biol. Evol. 25, 787–794 (2008)

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nick Lane.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lane, N., Martin, W. The energetics of genome complexity. Nature 467, 929–934 (2010). https://doi.org/10.1038/nature09486

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09486

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing