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.

  • Opinion
  • Published:

The early evolution of lipid membranes and the three domains of life

Abstract

All cell membranes are composed of glycerol phosphate phospholipids, and this commonality argues for the presence of such phospholipids in the last common ancestor, or cenancestor. However, phospholipid biosynthesis is very different between bacteria and archaea, leading to the suggestion that the cenancestor was devoid of phospholipid membranes. Recent phylogenomic studies challenge this view, suggesting that the cenancestor did possess complex phospholipid membranes. Here, we discuss the implications of these recent findings for membrane evolution in archaea and bacteria, and for the origin of the eukaryotic cell.

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

Access options

Buy this article

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

Figure 1: Phospholipid biosynthesis pathways in archaea, bacteria and eukaryotes.
Figure 2: Models explaining the early evolution of archaeal and bacterial phospholipid biosynthesis.
Figure 3: Complement of enzymes involved in the biosynthesis of phospholipid components in the cenancestor, and their evolution during the archaea–bacteria split.
Figure 4: Models explaining the bacterial-like nature of phospholipid membranes in eukaryotes.

Similar content being viewed by others

References

  1. Virchow, R. Die Cellularpathologie in ihrer Begründung auf physiologische und pathologische Gewebelehre. (Hirschwald, 1858).

    Google Scholar 

  2. Darwin, C. The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle For Life (John Murray, 1859).

    Google Scholar 

  3. Fitch, W. M. & Upper, K. The phylogeny of tRNA sequences provides evidence for ambiguity reduction in the origin of the genetic code. Cold Spring Harb. Symp. Quant. Biol. 52, 759–767 (1987).

    Article  CAS  PubMed  Google Scholar 

  4. Edidin, M. Lipids on the frontier: a century of cell-membrane bilayers. Nature Rev. Mol. Cell Biol. 4, 414–418 (2003).

    Article  CAS  Google Scholar 

  5. Pereto, J. Controversies on the origin of life. Int. Microbiol. 8, 23–31 (2005).

    CAS  PubMed  Google Scholar 

  6. Fry, I. The origins of research into the origins of life. Endeavour 30, 24–28 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. Mitchell, P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191, 144–148 (1961).

    Article  CAS  PubMed  Google Scholar 

  8. Kates, M., Yengoyan, L. S. & Sastry, P. S. A. diether analog of phosphatidyl glycerophosphate in Halobacterium cutirubrum. Biochim. Biophys. Acta 98, 252–268 (1965).

    Article  CAS  PubMed  Google Scholar 

  9. Langworthy, T. A., Smith, P. F. & Mayberry, W. R. Lipids of Thermoplasma acidophilum. J. Bacteriol. 112, 1193–1200 (1972).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Woese, C. R., Magrum, L. J. & Fox, G. E. Archaebacteria. J. Mol. Evol. 11, 245–251 (1978).

    Article  CAS  PubMed  Google Scholar 

  11. Koga, Y., Kyuragi, T., Nishihara, M. & Sone, N. Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J. Mol. Evol. 46, 54–63 (1998).

    Article  CAS  PubMed  Google Scholar 

  12. Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Rev. Microbiol. 1, 127–136 (2003).

    Article  CAS  Google Scholar 

  13. Szostak, J. W., Bartel, D. P. & Luisi, P. L. Synthesizing life. Nature 409, 387–390 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Martin, W. & Russell, M. J. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans. R. Soc. Lond. B 358, 59–83 (2003).

    Article  CAS  Google Scholar 

  15. Lowell, R. P., Rona, P. A. & Herzen, R. P. V. Seafloor hydrothermal systems. J. Geophys. Res. 100, 327–352 (1995).

    Article  CAS  Google Scholar 

  16. de Duve, C. The onset of selection. Nature 433, 581–582 (2005).

    Article  CAS  PubMed  Google Scholar 

  17. Wächtershäuser, G. From pre-cells to Eukarya – a tale of two lipids. Mol. Microbiol. 47, 13–22 (2003).

    Article  PubMed  Google Scholar 

  18. Damste, J. S. et al. Structural characterization of diabolic acid-based tetraester, tetraether and mixed ether/ester, membrane-spanning lipids of bacteria from the order Thermotogales. Arch. Microbiol. 188, 629–641 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Weijers, J. W. et al. Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ. Microbiol. 8, 648–657 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Kates, M., Wassef, M. K. & Kushner, D. J. Radioisotopic studies on the biosynthesis of the glyceryl diether lipids of Halobacterium cutirubrum. Can. J. Biochem. 46, 971–977 (1968).

    Article  CAS  PubMed  Google Scholar 

  21. Langworthy, T. A., Mayberry, W. R. & Smith, P. F. Long-chain glycerol diether and polyol dialkyl glycerol triether lipids of Sulfolobus acidocaldarius. J. Bacteriol. 119, 106–116 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Gattinger, A., Schloter, M. & Munch, J. C. Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling. FEMS Microbiol. Lett. 213, 133–139 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Lange, B. M., Rujan, T., Martin, W. & Croteau, R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl Acad. Sci. USA 97, 13172–13177 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. McGarvey, D. J. & Croteau, R. Terpenoid metabolism. Plant Cell 7, 1015–1026 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pereto, J., Lopez-Garcia, P. & Moreira, D. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29, 469–477 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. Lombard, J. & Moreira, D. Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol. Biol. Evol. 28, 87–99 (2011).

    Article  CAS  PubMed  Google Scholar 

  27. Lombard, J., López-García, P. & Moreira, D. An ACP-independent fatty acid synthesis pathway in archaea? Implications for the origin of phospholipids. Mol. Biol. Evol. (in the press).

  28. Lombard, J. & Moreira, D. Early evolution of the biotin-dependent carboxylase family. BMC Evol. Biol. 11, 232 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Soderberg, T., Chen, A. & Poulter, C. D. Geranylgeranylglyceryl phosphate synthase. Characterization of the recombinant enzyme from Methanobacterium thermoautotrophicum. Biochemistry 40, 14847–14854 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Hemmi, H., Shibuya, K., Takahashi, Y., Nakayama, T. & Nishino, T. (S)-2,3-Di-O-geranylgeranylglyceryl phosphate synthase from the thermoacidophilic archaeon Sulfolobus solfataricus. Molecular cloning and characterization of a membrane-intrinsic prenyltransferase involved in the biosynthesis of archaeal ether-linked membrane lipids. J. Biol. Chem. 279, 50197–50203 (2004).

    Article  CAS  PubMed  Google Scholar 

  31. Daiyasu, H. et al. A study of archaeal enzymes involved in polar lipid synthesis linking amino acid sequence information, genomic contexts and lipid composition. Archaea 1, 399–410 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jekely, G. Did the last common ancestor have a biological membrane? Biol. Direct 1, 35 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Gogarten, J. P. et al. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc. Natl Acad. Sci. USA 86, 6661–6665 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Brochier-Armanet, C., Talla, E. & Gribaldo, S. The multiple evolutionary histories of dioxygen reductases: implications for the origin and evolution of aerobic respiration. Mol. Biol. Evol. 26, 285–297 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Baymann, F. et al. The redox protein construction kit: pre-last universal common ancestor evolution of energy-conserving enzymes. Phil. Trans. R. Soc. Lond. B 358, 267–274 (2003).

    Article  CAS  Google Scholar 

  36. Lebrun, E. et al. The Rieske protein: a case study on the pitfalls of multiple sequence alignments and phylogenetic reconstruction. Mol. Biol. Evol. 23, 1180–1191 (2006).

    Article  CAS  PubMed  Google Scholar 

  37. Vignais, P. M., Billoud, B. & Meyer, J. Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25, 455–501 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Gribaldo, S. & Cammarano, P. The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J. Mol. Evol. 47, 508–516 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Cao, T. B. & Saier, M. H. Jr. The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim. Biophys. Acta 1609, 115–125 (2003).

    Article  CAS  PubMed  Google Scholar 

  40. Yen, M. R., Harley, K. T., Tseng, Y. H. & Saier, M. H. Jr. Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol. Lett. 204, 223–231 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Yen, M. R., Tseng, Y. H., Nguyen, E. H., Wu, L. F. & Saier, M. H. Jr. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177, 441–450 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Koonin, E. V. & Martin, W. On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y. & Koonin, E. V. Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nature Rev. Microbiol. 5, 892–899 (2007).

    Article  CAS  Google Scholar 

  44. Shimada, H. & Yamagishi, A. Stability of heterochiral hybrid membrane made of bacterial sn-G3P lipids and archaeal sn-G1P lipids. Biochemistry 50, 4114–4120 (2011).

    Article  CAS  PubMed  Google Scholar 

  45. Budin, I. & Szostak, J. W. Physical effects underlying the transition from primitive to modern cell membranes. Proc. Natl Acad. Sci. USA 108, 5249–5254 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Koga, Y. Early evolution of membrane lipids: how did the lipid divide occur? J. Mol. Evol. 72, 274–282 (2011).

    Article  CAS  PubMed  Google Scholar 

  47. Boussau, B., Blanquart, S., Necsulea, A., Lartillot, N. & Gouy, M. Parallel adaptations to high temperatures in the Archaean eon. Nature 456, 942–945 (2008).

    Article  CAS  PubMed  Google Scholar 

  48. Valentine, D. L. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nature Rev. Microbiol. 5, 316–323 (2007).

    Article  CAS  Google Scholar 

  49. Taron, D. J., Childs, W. C., 3rd & Neuhaus, F. C. Biosynthesis of D-alanyl-lipoteichoic acid: role of diglyceride kinase in the synthesis of phosphatidylglycerol for chain elongation. J. Bacteriol. 154, 1110–1116 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Itabashi, Y. & Kuksis, A. Reassessment of stereochemical configuration of natural phosphatidylglycerols by chiral-phase high-performance liquid chromatography and electrospray mass spectrometry. Anal. Biochem. 254, 49–56 (1997).

    Article  CAS  PubMed  Google Scholar 

  51. Kolbe, M., Besir, H., Essen, L. O. & Oesterhelt, D. Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution. Science 288, 1390–1396 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cavalier-Smith, T. Deep phylogeny, ancestral groups and the four ages of life. Phil. Trans. R. Soc. B 365, 111–132 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Junglas, B. et al. Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190, 395–408 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Gray, M. W. & Doolittle, W. F. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46, 1–42 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).

    Article  CAS  PubMed  Google Scholar 

  57. Poole, A. M. & Penny, D. Evaluating hypotheses for the origin of eukaryotes. Bioessays 29, 74–84 (2007).

    Article  PubMed  Google Scholar 

  58. Gribaldo, S., Poole, A. M., Daubin, V., Forterre, P. & Brochier-Armanet, C. The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature Rev. Microbiol. 8, 743–752 (2010).

    Article  CAS  Google Scholar 

  59. Lopez-Garcia, P. & Moreira, D. Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88–93 (1999).

    Article  CAS  PubMed  Google Scholar 

  60. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239–6244 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ribeiro, S. & Golding, G. B. The mosaic nature of the eukaryotic nucleus. Mol. Biol. Evol. 15, 779–788 (1998).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  64. Moreira, D. & Lopez-Garcia, P. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517–530 (1998).

    Article  CAS  PubMed  Google Scholar 

  65. Lopez-Garcia, P. & Moreira, D. Selective forces for the origin of the eukaryotic nucleus. Bioessays 28, 525–533 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Horiike, T., Hamada, K., Kanaya, S. & Shinozawa, T. Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homology-hit analysis. Nature Cell Biol. 3, 210–214 (2001).

    Article  CAS  PubMed  Google Scholar 

  67. Mansy, S. S. et al. Template-directed synthesis of a genetic polymer in a model protocell. Nature 454, 122–125 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Edgell, D. R. & Doolittle, W. F. Archaea and the origin(s) of DNA replication proteins. Cell 89, 995–998 (1997).

    Article  CAS  PubMed  Google Scholar 

  69. Rothfield, L., Taghbalout, A. & Shih, Y. L. Spatial control of bacterial division-site placement. Nature Rev. Microbiol. 3, 959–968 (2005).

    CAS  Google Scholar 

  70. Mileykovskaya, E. & Dowhan, W. Role of membrane lipids in bacterial division-site selection. Curr. Opin. Microbiol. 8, 135–142 (2005).

    Article  CAS  PubMed  Google Scholar 

  71. Tornabene, T. G. et al. Phytanyl-glycerol ethers and squalenes in the archaebacterium Methanobacterium thermoautotrophicum. J. Mol. Evol. 11, 259–266 (1978).

    Article  CAS  PubMed  Google Scholar 

  72. Tornabene, T. G. & Langworthy, T. A. Diphytanyl and dibiphytanyl glycerol ether lipids of methanogenic archaebacteria. Science 203, 51–53 (1979).

    Article  CAS  PubMed  Google Scholar 

  73. Monnard, P. A. & Deamer, D. W. Membrane self-assembly processes: steps toward the first cellular life. Anat. Rec. 268, 196–207 (2002).

    Article  CAS  PubMed  Google Scholar 

  74. Deamer, D. W. & Barchfeld, G. L. Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions. J. Mol. Evol. 18, 203–206 (1982).

    Article  CAS  PubMed  Google Scholar 

  75. Chen, I. A. & Szostak, J. W. Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. Proc. Natl Acad. Sci. USA 101, 7965–7970 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hanczyc, M. M. & Szostak, J. W. Replicating vesicles as models of primitive cell growth and division. Curr. Opin. Chem. Biol. 8, 660–664 (2004).

    Article  CAS  PubMed  Google Scholar 

  77. Oparin, A. I. The Origin of Life (Macmillan, 1938).

  78. Deamer, D. W. Boundary structures are formed by organic components of the Murchison carbonaceous chondrite. Nature 317, 792–794 (1985).

    Article  CAS  Google Scholar 

  79. Pohorille, A. & Deamer, D. Self-assembly and function of primitive cell membranes. Res. Microbiol. 160, 449–456 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Mansy, S. S. & Szostak, J. W. Reconstructing the emergence of cellular life through the synthesis of model protocells. Cold Spring Harb. Symp. Quant. Biol. 74, 47–54 (2009).

    Article  CAS  PubMed  Google Scholar 

  81. Segre, D., Ben-Eli, D., Deamer, D. W. & Lancet, D. The lipid world. Orig. Life Evol. Biosph. 31, 119–145 (2001).

    Article  CAS  PubMed  Google Scholar 

  82. Kandler, O. Cell wall biochemistry in archaea and its phylogenetic implications. J. Biol. Phys. 20, 165–169 (1994).

    Article  CAS  Google Scholar 

  83. Mulkidjanian, A. Y., Galperin, M. Y., Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Evolutionary primacy of sodium bioenergetics. Biol. Direct 3, 13 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the interdisciplinary programmes Origine des Planètes et de la Vie and InTerrVie (Interactions Terre/Vie, both of the French Centre National de la Recherche Scientifique and the French Institut National des Sciences de l'Univers. J.L. is a recipient of a Ph.D. fellowship from the French Research Ministry. The authors thank the anonymous referees for useful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Moreira.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

David Moreira's homepage

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lombard, J., López-García, P. & Moreira, D. The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10, 507–515 (2012). https://doi.org/10.1038/nrmicro2815

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2815

This article is cited by

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