Skip to main content
SpringerLink
Log in

Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Polar lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum was analyzed using terbinafine, an inhibitor of tetraether lipid biosynthesis. Cells of T. acidophilum were labeled with [14C]mevalonic acid, and their lipids were extracted and analyzed by two-dimensional thin-layer chromatography. Lipids labeled with [14C]mevalonic acid, [14C]glycerol, and [32P]orthophosphoric acid were extracted and hydrolyzed under different conditions to determine the structure of polar lipids. The polar lipids were estimated to be archaetidylglycerol, glycerophosphatidylcaldarchaetidylglycerol, caldarchaetidylglycerol, and β-l-gulopyranosylcaldarchaetidylglycerol, the main polar lipid of T. acidophilum. Pulse and chase experiments with terbinafine revealed that one tetraether lipid molecule is synthesized by head-to-head condensation of two molecules of archaetidylglycerol and that a sugar group of tetraether phosphoglycolipid is expected to attach to the tetraether lipid core after head-to-head condensation in T. acidophilum. A precursor accumulated in the presence of terbinafine with a fast-atom-bombardment mass spectrometry peak m/z 806 was compatible with archaetidylglycerol. The relative height of the peak m/z 806 decreased after removal of the inhibitor. The results suggest that most of the precursor, archaetidylglycerol, is in fully saturated form.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2a–f.
Fig. 3a, b.
Fig. 4.
Fig. 5.
Fig. 6a, b.

Similar content being viewed by others

References

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Chen A, Poulter CD (1993) Purification and characterization of farnesyl diphosphate/geranylgeranyl diphosphate synthase. A thermostable bifunctional enzyme from Methanobacterium thermoautotrophicum. J Biol Chem 268:11002–11007

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • De Rosa M, Gambacorta A, Nicolaus B, Chappe B, Albrecht P (1983) Isoprenoid ethers: backbone of complex lipids of the archaebacterium Sulfolobus solfataricus. Biochim Biophys Acta 753:249–256

    Google Scholar 

  • Eguchi T, Takyo H, Morita M, Kakinuma K, Koga Y (2000) Unusual double-bond migration as a plausible key reaction in the biosynthesis of the isoprenoidal membrane lipids of methanogenic archaea. Chem Commun 1545–1546

  • Ekiel I, Sprott GD (1992) Identification of degradation artifacts formed upon treatment of hydroxydiether lipids from methanogens with methanolic HCl. Can J Microbiol 38:764–768

    CAS  Google Scholar 

  • Koga Y, Nishihara M, Morii H, Akagawa-Matsushita M (1993) Ether polar lipids of methanogenic bacteria: structures, comparative aspects, and biosyntheses. Microbiol Rev 57:164–182

    CAS  PubMed  Google Scholar 

  • Kon T, Nemoto N, Oshima T, Yamagishi A (2002) Effects of a squalene epoxidase inhibitor, terbinafine, on ether lipid biosyntheses in a thermoacidophilic archaeon, Thermoplasma acidophilum. J Bacteriol 184:1395–1401

    CAS  PubMed  Google Scholar 

  • Kushwaha SC, Kates M, Sprott GD, Smith IC (1981) Novel polar lipids from the methanogen Methanospirillum hungatei GP1. Biochim Biophys Acta 664:156–173

    Article  CAS  PubMed  Google Scholar 

  • Langworthy TA (1982) Lipids of Thermoplasma. Methods Enzymol 88:396–406

    CAS  Google Scholar 

  • Langworthy TA, Smith, PF, Mayberry WR (1972) Lipids of Thermoplasma acidophilum. J Bacteriol 112:1193–1200

    CAS  PubMed  Google Scholar 

  • Moldoveanu N, Kates M (1988) Biosynthetic studies of the polar lipids of Halobacterium cutirubrum. Formation of isoprenyl ether intermediates. Biochim Biophys Acta 960:164–182

    Article  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  CAS  PubMed  Google Scholar 

  • Nishihara M, Morii H, Koga Y (1989) Heptads of polar ether lipids of an archaebacterium, Methanobacterium thermoautotrophicum: Structure and biosynthetic relationship. Biochemistry 28:95–102

    CAS  Google Scholar 

  • Ohnuma S, Suzuki M, Nishino T (1994) Archaebacterial ether-linked lipid biosynthetic gene. Expression cloning, sequencing, and characterization of geranylgeranyl-diphosphate synthase. J Biol Chem 269:14792–14797

    CAS  PubMed  Google Scholar 

  • Ross HMN, Grant WD (1985) Chemical methods in bacterial systematics. Wiley, New York

  • Ryder NS (1984) Microbial cell wall synthesis and autolysis. Elsevier, Amsterdam

  • Shimada H, Nemoto N, Shida Y, Oshima T, Yamagishi A (2002) Complete polar lipid composition of Thermoplasma acidophilum HO-62 determined by high-performance liquid chromatography with evaporative light-scattering detection. J Bacteriol 184:556–563

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Sugai A, Uda I, Kon K, Ando S, Itoh YH, Itoh T (1996) Structural identification of minor phosphoinositol lipids in Sulfolobus acidocaldarius N-8. J Jpn Oil Chem Soc 45:327–333

    CAS  Google Scholar 

  • Swain M, Brisson JR, Sprott GD, Cooper FP, Patel GB (1997) Identification of β-l-gulose as the sugar moiety of the main polar lipid Thermoplasma acidophilum. Biochim Biophys Acta 1345:56–64

    Article  CAS  PubMed  Google Scholar 

  • Tachibana A (1994) A novel prenyltransferase, farnesylgeranyl diphosphate synthase, from the haloalkaliphilic archaeon, Natronobacterium pharaonis. FEBS Lett 341:291–294

    Article  CAS  PubMed  Google Scholar 

  • Trincone A, De Rosa M, Gambacorta A, Lanzotti V, Nicolaus B, Harris JE, Grant WD (1988) A simple chromatographic procedure for the detection of cyclized archaebacterial glycerol-bisdiphytanyl-glycerol tetraether core lipids. J Gen Microbiol 134:3159–3163

    CAS  PubMed  Google Scholar 

  • Uda I, Sugai A, Kon K, Ando S, Itoh YH, Itoh T (1999) Isolation and characterization of novel neutral glycolipids from Thermoplasma acidophilum. Biochim Biophys Acta 1439:363–370

    Article  CAS  PubMed  Google Scholar 

  • Uda I, Sugai A, Itoh YH, Itoh T (2000a) Characterization of caldarchaetidylglycerol analogs, dialkyl-type and trialkyl-type, from Thermoplasma acidophilum. Lipids 35:1155–1157

    CAS  PubMed  Google Scholar 

  • Uda I, Sugai A, Shimizu A, Itoh YH, Itoh T (2000b) Glucosylcaldarchaetidylglycerol, a minor phosphoglycolipid from Thermoplasma acidophilum. Biochim Biophys Acta 1484:83–86

    Article  CAS  PubMed  Google Scholar 

  • Yasuda M, Oyaizu H, Yamagishi A, Oshima T (1995) Morphological variation of new Thermoplasma acidophilum isolates from Japanese hot springs. Appl Environ Microbiol 61:3482–3485

    CAS  PubMed  Google Scholar 

  • Zhang D, Poulter CD (1993) Biosynthesis of archaebacterial lipids in Halobacterium halobium and Methanobacterium thermoautotrophicum. J Org Chem 58:3919–3922

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (09839033).

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Tokyo University of Pharmacy and Life Science, 1432-1 Horinouchi, Hachioji, Tokyo 192-0392, Japan

    Naoki Nemoto, Haruo Shimada, Tairo Oshima & Akihiko Yamagishi

  2. Department of Chemical Analysis, Tokyo University of Pharmacy and Life Science, Tokyo, Japan

    Yasuo Shida

Authors
  1. Naoki Nemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasuo Shida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haruo Shimada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tairo Oshima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akihiko Yamagishi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akihiko Yamagishi.

Additional information

Communicated by G. Antranikian

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nemoto, N., Shida, Y., Shimada, H. et al. Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum . Extremophiles 7, 235–243 (2003). https://doi.org/10.1007/s00792-003-0315-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-003-0315-x

Keywords

Search

Navigation