Skip to main content
Log in

Enzyme-Driven Speciation: Crystallizing Archaea via Lipid Capture

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

As the origin(s) of life on Earth remains an open question, detailed characteristics about the “last universal ancestor” (LUA) continue to be obscured. Here we provide arguments that strengthen the bacterial-like nature of the LUA. Our view attempts to recreate the evolution of archaeal lipids, the major components of the distinctive membrane that encapsulates these ancient prokaryotes. We show that (S)- 3-O-geranylgeranylglyceryl phosphate synthase (GGGPS), a TIM-barrel protein that performs the committed step in archaeal lipid synthesis, likely evolved from the duplication and fusion of a (βα)4 half-barrel ancestor. By comparison to the well-characterized HisA and HisF TIM-barrel proteins, we propose a time line for the invention of this diagnostic archaeal biosynthetic pathway. After excluding the possibility of horizontal gene transfer, we conclude that the evolutionary history of GGGPS mirrors the emergence of Archaea from the LUA. We illustrate aspects of this “lipid capture” model that support its likelihood in recreating key evolutionary events and, as our hypothesis is built on a single initiating event, we suggest that the appearance of GGGPS represents an example of enzyme-driven speciation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Akashi H, Gojobori T (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99:3695–700

    Article  PubMed  CAS  Google Scholar 

  • Albers SV, van de Vossenberg JL, Driessen AJ, Konings WN (2000) Adaptations of the archaeal cell membrane to heat stress. Front Biosci 5:D813–D820

    PubMed  CAS  Google Scholar 

  • Albers SV, Szabó Z, Driessen AJ (2006) Protein secretion in the Archaea: multiple paths towards a unique cell surface. Nat Rev Microbiol 4:537–547

    Article  PubMed  CAS  Google Scholar 

  • Boucher Y, Kamekura M, Doolittle WF (2004) Origins and evolution of isoprenoid lipid biosynthesis in Archaea. Mol Microbiol 52:515–527

    Article  PubMed  CAS  Google Scholar 

  • Briones C, Manrubia SC, Lázaro E, Lazcano A, Amils R (2005) Reconstructing evolutionary relationships from functional data: a consistent classification of organisms based on translation inhibition response. Mol Phylogenet Evol 34:371–381

    Article  PubMed  CAS  Google Scholar 

  • Chen A, Zhang D, Poulter CD (1993) (S)-geranylgeranylglyceryl phosphate synthase. Purification and characterization of the first pathway-specific enzyme in archaebacterial membrane lipid biosynthesis. J Biol Chem 268:21701–21705

    PubMed  CAS  Google Scholar 

  • Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311:1283–1287

    Article  PubMed  CAS  Google Scholar 

  • Daiyasu H, Hiroike T, Koga Y, Toh H (2002) Analysis of membrane stereochemistry with homology modeling of sn-glycerol-1-phosphate dehydrogenase. Protein Eng 15:987–995

    Article  PubMed  CAS  Google Scholar 

  • Daiyasu H, Kuma K, Yokoi T, Morii H, Koga Y, Toh H (2005) A study of archaeal enzymes involved in polar lipid synthesis linking amino acid sequence information, genomic contexts and lipid composition. Archaea 1:399–410

    PubMed  CAS  Google Scholar 

  • De Rosa M, Gambacorta A, Gliozzi A (1986) Structure, biosynthesis, and physicochemical properties of archaebacterial lipids. Microbiol Rev 50:70–80

    PubMed  Google Scholar 

  • Eisenreich W, Bacher A, Arigoni D, Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61:1401–1426

    Article  PubMed  CAS  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630

    Article  PubMed  CAS  Google Scholar 

  • Fischer W, Arneth-Seifert D (1998) D-Alanylcardiolipin, a major component of the unique lipid pattern of Vagococcus fluvialis. J Bacteriol 180:2950–2957

    PubMed  CAS  Google Scholar 

  • Forterre P (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci USA 103:3669–3674

    Article  PubMed  CAS  Google Scholar 

  • Forterre P, Philippe H (1999) Where is the root of the universal tree of life? Bioessays 21:871–879

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Gil LJ, Gich FB, Fuentes-Garcia X (2003) A comparative study of bchG from green photosynthetic bacteria. Arch Microbiol 179:108–115

    PubMed  CAS  Google Scholar 

  • Gaspar JA, Liu C, Vassall KA, Meglei G, Stephen R, Stathopulos PB, Pineda-Lucena A, Wu B, Yee A, Arrowsmith CH, Meiering EM (2005) A novel member of the YchN-like fold: solution structure of the hypothetical protein Tm0979 from Thermotoga maritima. Protein Sci 14:216–223

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Glansdorff N (2000) About the last common ancestor, the universal life-tree and lateral gene transfer: a reappraisal. Mol Microbiol 38:177–185

    Article  PubMed  CAS  Google Scholar 

  • Glass JI, Assad-Garcia N, Alperovich N, Yooseph S, Lewis MR, Maruf M, Hutchison CA III, Smith HO, Venter JC (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci USA 103:425–430

    Article  PubMed  CAS  Google Scholar 

  • Graham DE, Overbeek R, Olsen GJ, Woese CR (2000) An archaeal genomic signature. Proc Natl Acad Sci USA 97:3304–3308

    Article  PubMed  CAS  Google Scholar 

  • Han JS, Ishikawa K (2005) Active site of Zn2+-dependent sn-glycerol-1-phosphate dehydrogenase from Aeropyrum pernix K1. Archaea 1:311–317

    Article  PubMed  CAS  Google Scholar 

  • Hemmi H, Shibuya K, Takahashi Y, Nakayama T, Nishino T (2004) (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

    Article  PubMed  CAS  Google Scholar 

  • Höcker B, Beismann-Driemeyer S, Hettwer S, Lustig A, Sterner R (2001) Dissection of a (βα)8-barrel enzyme into two folded halves. Nat Struct Biol 8:32–36

    Article  PubMed  Google Scholar 

  • Höcker B, Claren J, Sterner R (2004) Mimicking enzyme evolution by generating new (βα)8-barrels from (βα)4-half-barrels. Proc Natl Acad Sci USA 101:16448–16453

    Article  PubMed  CAS  Google Scholar 

  • Holm L, Sander C (1996) Mapping the protein universe. Science 273:595–603

    Article  PubMed  CAS  Google Scholar 

  • Hurst LD, Feil EJ, Rocha EP (2006) Protein evolution: causes of trends in amino-acid gain and loss. Nature 442:E11–E112

    Article  PubMed  CAS  Google Scholar 

  • Ishitani R, Nureki O, Fukai S, Kijimoto T, Nameki N, Watanabe M, Kondo H, Sekine M, Okada N, Nishimura S, Yokoyama S (2002) Crystal structure of archaeosine tRNA-guanine transglycosylase. J Mol Biol 318:665–677

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30:409–425

    Article  PubMed  CAS  Google Scholar 

  • Jordan IK, Kondrashov FA, Adzhubei IA, Wolf YI, Koonin EV, Kondrashov AS, Sunyaev S (2005) A universal trend of amino acid gain and loss in protein evolution. Nature 433:633–638

    Article  PubMed  CAS  Google Scholar 

  • Jordan IK, Kondrashov FA, Adzhubei IA, Wolf YI, Koonin EV, Kondrashov AS, Sunyaev S (2006) Protein evolution: causes of trends in amino-acid gain and loss—Reply. Nature 442:E12

    Article  CAS  Google Scholar 

  • Kandler O, König H (1998) Cell wall polymers in Archaea (Archaebacteria). Cell Mol Life Sci 54:305–308

    Article  PubMed  CAS  Google Scholar 

  • Kennedy EP, Rumley MK, Schulman H, van Golde LM (1976) Identification of sn-glycero-1-phosphate and phosphoethanolamine residues linked to the membrane-derived oligosaccharides of Escherichia coli. J Biol Chem 251:4208–4213

    PubMed  CAS  Google Scholar 

  • Kleywegt GJ (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr D Biol Crystallogr 52:842–857

    Article  PubMed  CAS  Google Scholar 

  • Koga Y, Morii H (2005) Recent advances in structural research on ether lipids from archaea including comparative and physiological aspects. Biosci Biotechnol Biochem 69:2019–2034

    Article  PubMed  CAS  Google Scholar 

  • Koga Y, Kyuragi T, Nishihara M, Sone N (1998) 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

    Article  PubMed  CAS  Google Scholar 

  • Koga Y, Sone N, Noguchi S, Morii H (2003) Transfer of pro-R hydrogen from NADH to dihydroxyacetonephosphate by sn-glycerol-1-phosphate dehydrogenase from the archaeon Methanothermobacter thermautotrophicus. Biosci Biotechnol Biochem 67:1605–1608

    Article  PubMed  CAS  Google Scholar 

  • Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Cryst 24:946–950

    Article  Google Scholar 

  • Kuper J, Doenges C, Wilmanns M (2005) Two-fold repeated (βα)4 half-barrels may provide a molecular tool for dual substrate specificity. EMBO Rep 6:134–139

    Article  PubMed  CAS  Google Scholar 

  • Kurland CG, Collins LJ, Penny D (2006) Genomics and the irreducible nature of eukaryote cells. Science 312:1011–1014

    Article  PubMed  CAS  Google Scholar 

  • Kuzuyama T, Noel JP, Richard SB (2005) Structural basis for the promiscuous biosynthetic prenylation of aromatic natural products. Nature 435:983–987

    Article  PubMed  CAS  Google Scholar 

  • Lang D, Thoma R, Henn-Sax M, Sterner R, Wilmanns M (2000) Structural evidence for evolution of the β/α barrel scaffold by gene duplication and fusion. Science 289:1546–1550

    Article  PubMed  CAS  Google Scholar 

  • Langer D, Hain J, Thuriaux P, Zillig W (1995) Transcription in Archaea: similarity to that in Eucarya. Proc Natl Acad Sci USA 92:5768–5772

    Article  PubMed  CAS  Google Scholar 

  • Leopoldseder S, Claren J, Jürgens C, Sterner R (2004) Interconverting the catalytic activities of (βα)8-barrel enzymes from different metabolic pathways: sequence requirements and molecular analysis. J Mol Biol 337:871–879

    Article  PubMed  CAS  Google Scholar 

  • Liang PH, Ko TP, Wang AH (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269:3339–3354

    Article  PubMed  CAS  Google Scholar 

  • Lin ECC (1976) Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol 30:535–578

    Article  PubMed  CAS  Google Scholar 

  • Martin W (2004) Pathogenic archaebacteria: do they not exist because archaebacteria use different vitamins? Bioessays 26:592–593

    Article  PubMed  Google Scholar 

  • Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41–45

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 358:59–83, discussion 83–85

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH (2006) Apparent trends of amino acid gain and loss in protein evolution due to nearly neutral variation. Mol Biol Evol 23:240–244

    Article  PubMed  CAS  Google Scholar 

  • Merritt EA, Murphy ME (1994) Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr D Biol Crystallogr 50:869–873

    Article  PubMed  CAS  Google Scholar 

  • Morii H, Koga Y (2003) CDP-2,3-di-O-geranylgeranyl-sn-glycerol:L-serine O-archaetidyltransferase (archaetidylserine synthase) in the methanogenic archaeon Methanothermobacter thermautotrophicus. J Bacteriol 185:1181–1189

    Article  PubMed  CAS  Google Scholar 

  • Morii H, Nishihara M, Koga Y (2000) CTP:2,3-di-O-geranylgeranyl-sn-glycero-1-phosphate cytidyltransferase in the methanogenic archaeon Methanothermobacter thermoautotrophicus. J Biol Chem 275:36568–36574

    Article  PubMed  CAS  Google Scholar 

  • Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R, Galperin MY (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103:13126–13131

    Article  PubMed  CAS  Google Scholar 

  • Nagano N, Orengo CA, Thornton JM (2002) One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol 321:741–765

    Article  PubMed  CAS  Google Scholar 

  • Näther DJ, Rachel R (2004) The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure and composition. Biochem Soc Trans 32:199–203

    Article  PubMed  Google Scholar 

  • Nemoto N, Oshima T, Yamagishi A (2003) Purification and characterization of geranylgeranylglyceryl phosphate synthase from a thermoacidophilic archaeon, Thermoplasma acidophilum. J Biochem (Tokyo) 133:651–657

    CAS  Google Scholar 

  • Nichols DS, Miller MR, Davies NW, Goodchild A, Raftery M, Cavicchioli R (2004) Cold adaptation in the antarctic archaeon Methanococcoides burtonii involves membrane lipid unsaturation. J Bacteriol 186:8508–8515

    Article  PubMed  CAS  Google Scholar 

  • Nisbet EG, Sleep NH (2001) The habitat and nature of early life. Nature 409:1083–1091

    Article  PubMed  CAS  Google Scholar 

  • Nishimura Y, Eguchi T (2006) Biosynthesis of archaeal membrane lipids: digeranylgeranylglycerophospholipid reductase of the thermoacidophilic archaeon Thermoplasma acidophilum. J Biochem (Tokyo) 139:1073–1081

    CAS  Google Scholar 

  • Paltauf F (1994) Ether lipids in biomembranes. Chem Phys Lipids 74:101–139

    Article  PubMed  CAS  Google Scholar 

  • Payandeh J, Fujihashi M, Gillon W, Pai EF (2006) The crystal structure of (S)-3-O-geranylgeranylglyceryl phosphate synthase reveals an ancient fold for an ancient enzyme. J Biol Chem 281:6070–6078

    Article  PubMed  CAS  Google Scholar 

  • Penny D, Poole A (1999) The nature of the last universal common ancestor. Curr Opin Genet Dev 9:672–677

    Article  PubMed  CAS  Google Scholar 

  • Peretó J, López-García P, Moreira D (2004) Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem Sci 29:469–477

    Article  PubMed  CAS  Google Scholar 

  • Ruzheinikov SN, Burke J, Sedelnikova S, Baker PJ, Taylor R, Bullough PA, Muir NM, Gore MG, Rice DW (2001) Glycerol dehydrogenase: structure, specificity, and mechanism of a family III polyol dehydrogenase. Structure 9:789–802

    Article  PubMed  CAS  Google Scholar 

  • Sacchettini JC, Poulter CD (1997) Creating isoprenoid diversity. Science 277:1788–1789

    Article  PubMed  CAS  Google Scholar 

  • Sakasegawa S, Hagemeier CH, Thauer RK, Essen LO, Shima S (2004) Structural and functional analysis of the gpsA gene product of Archaeoglobus fulgidus: a glycerol-3-phosphate dehydrogenase with an unusual NADP+ preference. Protein Sci 13:3161–3171

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Hopmans EC, Pancost RD, Damsté JS (2000) Widespread occurrence of structurally diverse tetraether membrane lipids: evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. Proc Natl Acad Sci USA 97:14421–14426

    Article  PubMed  CAS  Google Scholar 

  • Segré D, Ben-Eli D, Deamer DW, Lancet D (2001) The lipid world. Orig Life Evol Biosph 31:119–145

    Article  PubMed  Google Scholar 

  • Shineberg B, Young IG (1976) Biosynthesis of bacterial menaquinones: the membrane-associated 1,4-dihydroxy-2-naphthoate octaprenyltransferase of Escherichia coli. Biochemistry 15:2754–2758

    Article  PubMed  CAS  Google Scholar 

  • Silverman JA, Balakrishnan R, Harbury PB (2001) Reverse engineering the (β/α)8 barrel fold. Proc Natl Acad Sci USA 98:3092–3097

    Article  PubMed  CAS  Google Scholar 

  • Simonson AB, Servin JA, Skophammer RG, Herbold CW, Rivera MC, Lake JA (2005) Decoding the genomic tree of life. Proc Natl Acad Sci USA 102(Suppl 1):6608–6613

    Article  PubMed  CAS  Google Scholar 

  • Soderberg T, Chen A, Poulter CD (2001) Geranylgeranylglyceryl phosphate synthase. Characterization of the recombinant enzyme from Methanobacterium thermoautotrophicum. Biochemistry 40:14847–14854

    Article  PubMed  CAS  Google Scholar 

  • Sterner R, Höcker B (2005) Catalytic versatility, stability, and evolution of the (βα)8-barrel enzyme fold. Chem Rev 105:4038–4055

    Article  PubMed  CAS  Google Scholar 

  • Suvarna K, Stevenson D, Meganathan R, Hudspeth ME (1998) Menaquinone (vitamin K2) biosynthesis: localization and characterization of the menA gene from Escherichia coli. J Bacteriol 180:2782–2787

    PubMed  CAS  Google Scholar 

  • Tice MM, Lowe DR (2004) Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431:549–552

    Article  PubMed  CAS  Google Scholar 

  • Vetsigian K, Woese C, Goldenfeld N (2006) Collective evolution and the genetic code. Proc Natl Acad Sci USA 103:10696–10701

    Article  PubMed  CAS  Google Scholar 

  • Wachtershäuser G (1988) Before enzymes and templates: theory of surface metabolism. Microbiol Rev 52:452–484

    PubMed  Google Scholar 

  • Wachtershäuser G (2003) From pre-cells to Eukarya—a tale of two lipids. Mol Microbiol 47:13–22

    Article  PubMed  Google Scholar 

  • Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859

    Article  PubMed  CAS  Google Scholar 

  • Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Doolittle RF, Bourne PE (2005) Phylogeny determined by protein domain content. Proc Natl Acad Sci USA 102:373–378

    Article  PubMed  CAS  Google Scholar 

  • Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414

    PubMed  CAS  Google Scholar 

  • Zhang H, Shibuya K, Hemmi H, Nishino T, Prestwich GD (2006) Total synthesis of geranylgeranylglyceryl phosphate enantiomers: substrates for characterization of 2,3-O-digeranylgeranylglyceryl phosphate synthase. Org Lett 8:943–946

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Given the nature of this report, we apologize for not citing or discussing many relevant contributions by a great number of authors. J.P. is grateful to Emily Cowan, Wing Lau, and Wanda Gillon for their support. We thank Dr. Masahiro Fujihashi for his assistance, and Drs. Ayeda Ayed, Ahmad Khorchid, and Michael Plevin for their comments on the manuscript. We appreciate the guidance of Drs. Niles Lehman, Martin Kreitman, and our anonymous referees. This work was supported by the Canada Research Chairs Program, the National Sciences and Engineering Research Council of Canada, and the Canadian Institutes of Health Research (E.F.P.).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jian Payandeh or Emil F. Pai.

Additional information

Reviewing Editor: Dr. Niles Lehman

Rights and permissions

Reprints and permissions

About this article

Cite this article

Payandeh, J., Pai, E.F. Enzyme-Driven Speciation: Crystallizing Archaea via Lipid Capture. J Mol Evol 64, 364–374 (2007). https://doi.org/10.1007/s00239-006-0141-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-006-0141-8

Keywords

Navigation