Skip to main content
SpringerLink
Log in

Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid

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

Abstract

Ferroplasma acidarmanus thrives in hot, extremely low pH, metal-rich solutions associated with dissolving metal sulfide ore deposits. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and thin layer chromatography analyses of F. acidarmanus membranes indicate that tetraether lipids predominate, with at least three core lipid structures. NMR measurements indicate that the cytoplasmic pH of F. acidarmanus is ~5.6. The optimal growth pH is ~1.2, and the lowest growth pH is ~0.0. Thus, these organisms maintain pH gradients across their membranes that approach 5 pH units. Tetraether lipids were originally thought to be specifically associated with thermophiles but are now known to be widely distributed within the archaeal domain. Our data, in combination with recently published results for thermophilic and mesothermophilic acidophilic archaea, indicate that there may be a stronger association between tetraether lipids and tolerance to acid and/or large metal ion gradients.

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. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Batrakov SG, Pivovarova TA, Esipov SE, Sheichenko VI, Karavaiko GI (2002) Beta-D-glucopyranosyl caldarchaetidylglycerol is the main lipid of the acidophilic, mesophilic, ferrous iron-oxidising archaeon Ferroplasma acidiphilum. Biochim Biophys Acta 1581:29–35

    Article  CAS  PubMed  Google Scholar 

  • Blochl E, Rachel R, Burggraf S, Hafenbradl D, Jannasch HW, Stetter KO (1997) Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 degrees C. Extremophiles 1:14–21

    Article  CAS  PubMed  Google Scholar 

  • Burton NP, Norris PR (2000) Microbiology of acidic, geothermal springs of Montserrat: environmental rDNA analysis. Extremophiles 4:315–320

    Article  CAS  PubMed  Google Scholar 

  • Comita PB, Gagosian RB, Pang H, Costello CE (1984) Structural elucidation of a unique macrocyclic membrane lipid from a new, extremely thermophilic, deep-sea hydrothermal vent archaebacterium, Methanococcus jannaschii. J Biol Chem 259:15234–15241

    CAS  PubMed  Google Scholar 

  • Corcelli A, Colella M, Mascolo G, Fanizzi FP, Kates M (2000) A novel glycolipid and phospholipid in the purple membrane. Biochemistry 39:3318–3326

    Article  CAS  PubMed  Google Scholar 

  • De Rosa M, Gambacorta A, Lanzotti V, Trincone A, Harris JE, Grant WD (1986) A range of ether core lipids from the methanogenic archaebacterium Methanosarcina barkeri. Biochimica Biophys Acta 875:487–492

    Google Scholar 

  • De Rosa M, Gambacorta A, Trincone A, Basso A, Zillig W, Holz I (1987) Lipids of Thermococcus celer, a sulfur-reducing archaebacterium: structure and biosynthesis. Syst Appl Microbiol 9:1–5

    Google Scholar 

  • De Vossenberg JLCM van, Driessen AJM, Konings WN (1998) The essence of being extremophilic: The role of the unique archaeal membrane lipids. Extremophiles 2:163–170

    Article  PubMed  Google Scholar 

  • DeLong EF, King LL, Massana R, Cittone H, Murray A, Schleper C, Wakeham SG (1998) Dibiphytanyl ether lipids in nonthermophilic crenarchaeotes. Appl Environ Microbiol 64:1133–1138

    CAS  PubMed  Google Scholar 

  • Edwards KJ, Schrenk MO, Hamers R, Banfield JF (1998) Microbial oxidation of pyrite: Experiments using microorganisms from an extreme acidic environment. Am Mineral 83:1444–1453

    CAS  Google Scholar 

  • Edwards KJ, Gihring TM, Banfield JF (1999) Seasonal variations in microbial populations and environmental conditions in an extreme acid mine drainage environment. Appl Environ Microbiol 65:3627–3632

    CAS  PubMed  Google Scholar 

  • Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799

    Article  CAS  PubMed  Google Scholar 

  • Ferrante G, Ekiel I, Sprott GD (1986) Structural characterization of the lipids of Methanococcus voltae, including a novel N-acetylglucosamine 1-phosphate diether. J Biol Chem 261:17062–17066

    CAS  PubMed  Google Scholar 

  • Ferrante G, Ekiel I, Patel GB, Sprott GD (1988) A novel core lipid isolated from the aceticlastic methanogen Methanothrix concilii GP6. Biochim Biophys Acta 963:173–182

    Article  CAS  Google Scholar 

  • Ferrante G, Richards JC, Sprott GD (1990) Structures of polar lipids from the thermophilic, deep-sea archaeobacterium Methanococcus jannaschii. Biochem Cell Biol 68:274–283

    CAS  PubMed  Google Scholar 

  • Gabriel JL, Chong PLG (2000) Molecular modeling of archaebacterial bipolar tetraether lipid membranes. Chem Phys Lipids 105:193–200

    Article  CAS  PubMed  Google Scholar 

  • Golyshina OV, Pivovarova TA, Karavaiko GI, Kondrat‘eva TF, Moore ERB, Abraham W-R, Luensdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50:997–1006

    CAS  PubMed  Google Scholar 

  • Hezayen FF, Tindall BJ, Steinbuechel A, Rehm BHA (2002) Characterization of a novel halophilic archaeon, Halobiforma haloterrestris gen. nov., sp. nov., and transfer of Natronobacterium nitratireducens to Halobiforma nitratireducens comb. nov. Int J Syst Evol Microbiol 52:2271–2280

    Article  CAS  PubMed  Google Scholar 

  • Hoefs MJL, Schouten S, De Leeuw JW, King LL, Wakeham SG, Damste JSS (1997) Ether lipids of planktonic archaea in the marine water column. Appl Environ Microbiol 63:3090–3095

    CAS  Google Scholar 

  • Hopmans EC, Schouten S, Pancost RD, van der Meer MTJ, Sinninghe Damste JS (2000) Analysis of intact tetraether lipids in archaeal cell material and sediments by high performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry. Rapid Commun Mass Spectrom 14:585–589

    Article  CAS  PubMed  Google Scholar 

  • Huber R, Dyba D, Huber H, Burggraf S, Rachel R (1998) Sulfur-inhibited Thermosphaera aggregans sp. nov., a new genus of hyperthermophilic archaea isolated after its prediction from environmentally derived 16S rRNA sequences. Int J Syst Bacteriol 48:31–38

    CAS  PubMed  Google Scholar 

  • Huber H, Burggraf S, Mayer T, Wyschkony I, Rachel R, Stetter KO (2000) Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov. and Ignicoccus pacificus sp. nov. Int J Syst Evol Microbiol 50:2093–2100

    PubMed  Google Scholar 

  • Itoh YH, Kurosawa N, Uda I, Sugai A, Tanoue S, Itoh T, Horiuchi T (2001) Metallosphaera sedula TA-2, a calditoglycerocaldarchaeol deletion strain of a thermoacidophilic archaeon. Extremophiles 5:241–245

    Article  CAS  PubMed  Google Scholar 

  • Kessel M, Volker S, Santarius U, Huber R, Baumeister W (1990) Three-dimensional reconstruction of the surface protein of the extremely thermophilic archaebacterium Archaeoglobus fulgidus. Syst Appl Microbiol 13:207–213

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lanzotti V, De Rosa M, Trincone A, Basso AL, Gambacorta A, Zillig W (1987) Complex Lipids from Desulfurococcus mobilis a sulfur-reducing Archaebacterium. Biochim Biophys Acta 922:95–102

    Article  CAS  Google Scholar 

  • Lanzotti V, Nicolaus B, Trincone A, Grant WD (1988) The glycolipid of Halobacterium saccharovorum. FEMS Microbiol Lett 55:223–228

    CAS  Google Scholar 

  • Lanzotti V, Trincone A, Nicolaus B, Zillig W, De Rosa M, Gambacorta A (1989) Complex lipids of Pyrococcus and AN1, thermophilic members of archaebacteria belonging to Thermococcales. Biochim Biophys Acta 1004:44–48

    Article  CAS  Google Scholar 

  • Lattuati A, Guezennec J, Metzger P, Largeau C (1998) Lipids of Thermococcus hydrothermalis, an archaea isolated from a deep-sea hydrothermal vent. Lipids 33:319–326

    CAS  PubMed  Google Scholar 

  • Lizama C, Monteoliva-Sanchez M, Suarez-Garcia A, Rosello-Mora R, Aguilera M, Campos V, Ramos-Cormenzana A (2002) Halorubrum tebenquichense sp. nov., a novel halophilic archaeon isolated from the Atacama Saltern, Chile. Int Syst Evol Microbiol 52:149–155

    CAS  Google Scholar 

  • Lundberg P, Harmsen E, Ho C, Vogel HJ (1990) NMR studies of cellular metabolism. Anal Biochem 191:193–222

    CAS  PubMed  Google Scholar 

  • Macalady J, Croft L, Vestling M, Harms A, Zheng L, Barry A, Baumler D, Kaspar C, Fox B, Banfield JF (2002) Tetraether-linked membrane lipids are essential for archaeal life in acid. Abstr Gen Meet Am Soc Microbiol 102:321

    Google Scholar 

  • Montalvo-Rodriguez R, Lopez-Garriga J, Vreeland RH, Oren A, Ventosa A, Kamekura M (2000) Haloterrigena thermotolerans sp. nov., a halophilic archaeon from Puerto Rico. Int J Syst Evol Microbiol 50:1065–1071

    CAS  PubMed  Google Scholar 

  • Moon RB, Richards JH (1972) Conformational studies of various hemoglobins by natural-abundance C13 NMR spectroscopy. Proc Natl Acad Sci USA 69:2193

    CAS  PubMed  Google Scholar 

  • Morii H, Eguchi T, Nishihara M, Kakinuma K, Konig H, Koga Y (1998) A novel ether core lipid with H-shaped C80-isoprenoid hydrocarbon chain from the hyperthermophilic methanogen Methanothermus fervidus. Biochim Biophys Acta 1390:339–345

    Article  CAS  PubMed  Google Scholar 

  • Morii H, Yagi H, Akutsu H, Nomura N, Sako Y, Koga Y (1999) A novel phosphoglycolipid archaetidyl(glucosyl)inositol with two sesterterpanyl chains from the aerobic hyperthermophilic archaeon Aeropyrum pernix K1. Biochim Biophys Acta 1436:426–436

    Article  CAS  PubMed  Google Scholar 

  • Nagle JF, Morowitz HJ (1978) Molecular mechanisms for proton transport in membranes. Proc Natl Acad Sci USA 75:298–302

    CAS  PubMed  Google Scholar 

  • Nichols PD, Franzmann PD (1992) Unsaturated diether phospholipids in the Antarctic methanogen Methanococcoides burtonii. FEMS Microbiol Lett 98:205–208

    Article  CAS  Google Scholar 

  • Nishihara M, Morii H, Matsuno K, Ohga M, Stetter KO, Koga Y (2002) Structural analysis by reductive cleavage with LiAlH4 of an allyl ether choline-phospholipid, archaetidylcholine, from the hyperthermophilic methanoarchaeon Methanopyrus kandleri. Archaea 1:123–131

    CAS  Google Scholar 

  • Okibe N, Garicke M, Hallberg KB, Johnson DB (2003) Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943

    Article  CAS  PubMed  Google Scholar 

  • Oren A, Gurevich P, Gemmell RT, Teske A (1995) Halobaculum gomorrense gen. nov., sp. nov., a novel extremely halophilic archaeon from the Dead Sea. Int J Syst Bacteriol 45:747–754

    CAS  PubMed  Google Scholar 

  • Oren A, Ventosa A, Gutierrez MC, Kamekura M (1999) Haloarcula quadrata sp. nov., a square, motile archaeon isolated from a brine pool in Sinai (Egypt). Int J Syst Bacteriol 49:1149–1155

    CAS  PubMed  Google Scholar 

  • Petroff OA, Prichard JW, Behar KL, Alger JR, Hollander JR, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35:781–788

    CAS  PubMed  Google Scholar 

  • Pivovarova TA, Kondrat’eva TF, Batrakov SG, Esipov SE, Sheichenko VI, Bykova SA, Lysenko AM, Karavaiko GI (2002) Phenotypic features of Ferroplasma acidiphilum strains YT and Y-2. Mikrobiologiya 71:809–818

    CAS  Google Scholar 

  • Qiu D-F, Games MPL, Xiao X-Y, Games DE, Walton TJ (1998) Application of high-performance liquid chromatography/electrospray mass spectrometry for the characterization of membrane lipids in the haloalkaliphilic archaebacterium Natronobacterium magadii. Rapid Commun Mass Spectrom 12:939–946

    Article  CAS  Google Scholar 

  • Qiu DF, Games MPL, Xiao XY, Games DE, Walton TJ (2000) Characterisation of membrane phospholipids and glycolipids from a halophilic archaebacterium by high-performance liquid chromatography/electrospray mass spectrometry. Rapid Commun Mass Spectrom 14:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Sako Y, Nomura N, Uchida A, Ishida Y, Morii H, Koga Y, Hoaki T, Maruyama T (1996) Aeropyrum pernix gen. nov., sp. nov., a novel aerobic hyperthermophilic archaeon growing at temperatures up to 100 degree C. Int J Syst Bacteriol 46:1070–1077

    CAS  PubMed  Google Scholar 

  • Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk H-P, Zillig W (1995) Picrophilus gen. nov., fam. nov.: A novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059

    CAS  PubMed  Google Scholar 

  • 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 

  • Sprott GD, Ekiel I, Dicaire C (1990) Novel, acid-labile, hydroxydiether lipid cores in methanogenic bacteria. J Biol Chem 265:13735–13740

    CAS  PubMed  Google Scholar 

  • Sprott GD, Dicaire CJ, Patel GB (1994a) The ether lipids of Methanosarcina mazei and other Methanosarcina species, compared by fast atom bombardment mass spectrometry. Can J Microbiol 40:837–843

    CAS  Google Scholar 

  • Sprott GD, Ferrante G, Ekiel I (1994b) Tetraether lipids of Methanospirillum hungatei with head groups consisting of phospho-N,N-dimethylaminopentanetetrol, phospho-N,N,N-trimethylaminopentanetetrol, and carbohydrates. Biochim Biophys Acta 1214:234–242

    Article  CAS  PubMed  Google Scholar 

  • Sprott GD, Agnew BJ, Patel GB (1997) Structural features of ether lipids in the archaeobacterial thermophiles Pyrococcus furiosus, Methanopyrus kandleri, Methanothermus fervidus, and Sulfolobus acidocaldarius. Can J Microbiol 43:467–476

    CAS  Google Scholar 

  • Sprott G, Krishnan L, Dicaire C, Patel G (1999) Liposomes composed of archaeobacterial polar lipids strongly stimulate both humoral and cell-mediated immune responses to an entrapped protein, in BALB/c mice. Abstr Gen Meet Am Soc Microbiol 99:276

    Google Scholar 

  • Swain M, Brisson J-R, Sprott GD, Cooper FP, Patel GB (1997) Identification of beta-lt-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 

  • Takai K, Sugai A, Itoh T, Horikoshi K (2000) Palaeococcus ferrophilus gen. nov., sp. nov., a barophilic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 50:489–500

    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 134:3159–3164

    CAS  PubMed  Google Scholar 

  • Trincone A, Lanzotti V, Nicolaus B, Zillig W, De Rosa M, Gambacorta A (1989) Comparative lipid composition of aerobically and anaerobically grown Desulfurolobus ambivalens, an autotrophic thermophilic archaebacterium. J Gen Microbiol 135:2751–2758

    CAS  Google Scholar 

  • Trincone A, Nicolaus B, Palmieri G, De Rosa M, Huber R, Huber G, Stetter KO, Gambacorta A (1992) Distribution of complex and core lipids within new hyperthermophilic members of the Archaea domain. Syst Appl Microbiol 15:11–17

    CAS  Google Scholar 

  • Uda I, Sugai A, Itoh YH, Itoh T (2001) Variation in molecular species of polar lipids from Thermoplasma acidophilum depends on growth temperature. Lipids 36:103–105

    CAS  PubMed  Google Scholar 

  • Vasquez M, Moore ERB, Espejo RT (1999) Detection by polymerase chain reaction amplification and sequencing of an archaeon in a commercial-scale copper bioleaching plant. FEMS Microbiol Lett 173:183–187

    Article  CAS  Google Scholar 

  • Volkl P, Huber R, Drobner E, Rachel R, Burggraf S, Trincone A, Stetter KO (1993) Pyrobaculum aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl Environ Microbiol 59:2918–2926

    CAS  PubMed  Google Scholar 

  • Xu Y, Zhou P, Tian X (1999) Characterization of two novel haloalkaliphilic archaea Natronorubrum bangense gen. nov., sp. nov. and Natronorubrum tibetense gen. nov., sp. nov. Int J Syst Bacteriol 49:261–266

    CAS  PubMed  Google Scholar 

  • Zillig W, Gierl A, Schreiber G, Wunderl S, Janekovic D, Stetter KO, Klenk HP (1983) The Archaebacterium Thermofilum pendens represents a novel genus of the thermophilic anaerobic sulfur respiring Thermoproteales. Syst Appl Microbiol 4:79–87

    Google Scholar 

Download references

Acknowledgements

A total lipid extract of H. saccharovorum was kindly provided by Dr. Linda Jahnke, NASA Ames Research Center, Ames, Calif. We also thank Mark E. Anderson of the University of Wisconsin NMR facility for his assistance in NMR measurements. Funding was provided by NSF LExEN grant number MC9978205, NSF EGB grant number CHE 9807598, and DOE Microbial Genomics Program grant number ER63160-1017457-0007147.

Author information

Author notes

  1. Jennifer L. Macalady

    Present address: Geology Department, Carleton College, One North College Street, Northfield, MN 55057, USA

Authors and Affiliations

  1. Department of Earth and Planetary Sciences, University of California Berkeley, McCone Hall, Berkeley, CA 94720-4767, USA

    Jennifer L. Macalady & Jillian F. Banfield

  2. Chemistry Department, University of Wisconsin Madison, 1101 University Avenue, Madison, WI 53706-1396, USA

    Martha M. Vestling

  3. Department of Food Microbiology and Toxicology, University of Wisconsin Madison, 1925 Willow Drive, Madison, WI 53706-1692, USA

    David Baumler & Charles W. Kaspar

  4. Geology Department, Carleton College, One North College Street, Northfield, MN 55057, USA

    Nick Boekelheide

  5. Department of Environmental Science, Policy and Management, University of California Berkeley, 369 McCone Hall, Berkeley, CA 94720-4767, USA

    Jillian F. Banfield

Authors
  1. Jennifer L. Macalady
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martha M. Vestling
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Baumler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nick Boekelheide
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Charles W. Kaspar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jillian F. Banfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer L. Macalady.

Additional information

Communicated by K. Horikoshi

Rights and permissions

Reprints and permissions

About this article

Cite this article

Macalady, J.L., Vestling, M.M., Baumler, D. et al. Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 8, 411–419 (2004). https://doi.org/10.1007/s00792-004-0404-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-004-0404-5

Keywords

Search

Navigation