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The major lipid cores of the archaeon Ignisphaera aggregans: implications for the phylogeny and biosynthesis of glycerol monoalkyl glycerol tetraether isoprenoid lipids

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Abstract

The lipid cores from Ignisphaera aggregans, a hyperthermophilic Crenarchaeon recently isolated from New Zealand hot springs, have been profiled by liquid chromatography–tandem mass spectrometry. The distribution revealed includes relatively high proportions of monoalkyl (also known as H-shaped) tetraether cores which have previously been implicated as kingdom-specific biomarkers for the Euryarchaeota. Such high expression of monoalkyl tetraether lipids is unusual in the archaeal domain and may indicate that formation of these components is an adaptive mechanism that allows I. aggregans to regulate membrane behaviour at high temperatures. The observed dialkyl tetraether and monoalkyl tetraether lipid distributions are similar but not fully concordant, showing differences in the average number of incorporated rings. The similarity supports a biosynthetic route to the ring-containing dialkyl and monoalkyl tetraether lipids via a dialkyl tetraether core containing zero rings, or a closely related structural relative, as an intermediate. Currently, however, the precise nature of the biosynthetic route to these lipids cannot be deduced.

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Abbreviations

CID:

Collision-induced dissociation

Cp:

Cyclopentyl

Da:

Daltons

DCM:

Dichloromethane

GDD:

Glycerol dialkyl diether

GDGT:

Glycerol dialkyl glycerol tetraether

GMD:

Glycerol monoalkyl diether

GMGT:

Glycerol monoalkyl glycerol tetraether

GTGT:

Glycerol trialkyl glycerol tetraether

LC–MS/MS:

Liquid chromatography–tandem mass spectrometry

[M+H]+ :

Protonated molecule

APCI:

Atmospheric pressure chemical ionisation

ESI:

Electrospray ionisation

References

  • Boyd ES, Pearson A, Pi Y, Li W-J, Zhang YG, He L, Zhang CL, Geesey GG (2011) Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens. Extremophiles 15:59–65

    Article  PubMed  CAS  Google Scholar 

  • Comita PB, Gagosian RB (1983) Membrane lipid from deep-sea hydrothermal vent methanogen—a new macrocyclic glycerol diether. Science 222:1329–1331

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Damsté JSS, Schouten S, Hopmans EC, van Duin ACT, Geenevasen JAJ (2002) Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lip Res 43:1641–1651

    Article  Google Scholar 

  • de la Torre J, Walker CB, Ingalls AE, Könneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  Google Scholar 

  • De Rosa M, Gambacorta A (1988) The lipids of Archaebacteria. Prog Lipid Res 27:153–175

    Article  PubMed  Google Scholar 

  • De Rosa M, Gambacorta A, Nicolaus B, Sodano S, Bu’Lock JD (1980a) Structural regularities in tetraether lipids of Caldariella and their biosynthetic and phyletic implications. Phytochemistry 19:833–836

    Article  Google Scholar 

  • De Rosa M, Esposito E, Gambacorta A, Nicolaus B, Bu’Lock JD (1980b) Effects of temperature on ether lipid composition of Caldariella acidophila. Phytochemistry 19:827–831

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Eguchi T, Nishimura Y, Kakinuma K (2003) Importance of the isopropylidene terminal of geranylgeranyl group for the formation of tetraether lipids in methanogenic archaea. Tetrahedron Lett 44:3275–3279

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gattinger A, Günthner A, Schloter M, Munch JC (2003) Characterisation of Archaea in soils by polar lipid analysis. Acta Biotechnol 23:21–28

    Article  CAS  Google Scholar 

  • Gliozzi A, Relini A, Chong PL-G (2002) Structure and permeability properties of biomimetic membranes of bolaform archaeal tetraether lipids. J Membr Sci 206:131–147

    Article  CAS  Google Scholar 

  • Gräther O, Arigoni D (1995) Detection of regioisomeric macrocyclic tetraethers in the lipids of Methanobacterium thermoautotrophicum and other archaeal organisms. J Chem Soc Chem Commun 4:405–406

    Article  Google Scholar 

  • Hopmans EC, Schouten S, Pancost RD, van der Meer MTJ, Damsté JSS (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  PubMed  CAS  Google Scholar 

  • Kates M (1972) Ether-linked lipids in extremely halophilic bacteria. In: Snyder F (ed) Ether lipids: chemistry and biology. Academic Press, New York, pp 351–398

    Google Scholar 

  • Kim J-H, Schouten S, Hopmans EC, Donner B, Damsté JSS (2008) Global sediment core-top calibration of the TEX86 paleothermometer in the ocean. Geochim Cosmochim Acta 72:1154–1173

    Article  CAS  Google Scholar 

  • Knappy CS (2010) Mass spectrometric studies of ether lipids in Archaea and sediments. PhD thesis, University of York, UK

  • Knappy CS, Chong JPJ, Keely BJ (2009) Rapid discrimination of archaeal tetraether lipid cores by liquid chromatography–tandem mass spectrometry. J Am Soc Mass Spectrom 20:51–59

    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, Morii H (2006) Special methods for the analysis of ether lipid structure and metabolism in archaea. Anal Biochem 348:1–14

    Article  PubMed  CAS  Google Scholar 

  • Koga Y, Morii H (2007) Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71:97–120

    Article  PubMed  CAS  Google Scholar 

  • Koga Y, Akagawa-Matsushita M, Ohga M, Nishihara M (1993) Taxonomic significance of the distribution of component parts of polar ether lipids in methanogens. Syst Appl Microbiol 16:342–351

    CAS  Google Scholar 

  • Lai D, Springstead JR, Monbouquette HG (2008) Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus. Extremophiles 12:271–278

    Article  PubMed  CAS  Google Scholar 

  • Lutnaes BF, Brandal Ø, Sjöblom J, Krane J (2006) Archaeal C80 isoprenoid tetraacids responsible for naphthenate deposition in crude oil processing. Org Biomol Chem 4:616–620

    Article  PubMed  CAS  Google Scholar 

  • Lutnaes BF, Krane J, Smith BE, Rowland SJ (2007) Structure elucidation of C80, C81 and C82 isoprenoid tetraacids responsible for naphthenate deposition in crude oil production. Org Biomol Chem 5:1873–1877

    Article  PubMed  CAS  Google Scholar 

  • Mancuso CA, Nichols PD, White DC (1986) A method for the separation and characterization of archaebacterial signature ether lipids. J Lipid Res 27:49–56

    PubMed  CAS  Google Scholar 

  • Matsuno Y, Sugai A, Higashibata H, Fukuda W, Ueda K, Uda I, Sato I, Itoh T, Imanaka T, Fujiwara S (2009) Effect of growth temperature and growth phase on the lipid composition of the archaeal membrane from Thermococcus kodakaraensis. Biosci Biotechnol Biochem 73:104–108

    Article  PubMed  CAS  Google Scholar 

  • Morii H, Eguchi T, Nishihara M, Kakinuma K, König 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

    PubMed  CAS  Google Scholar 

  • Nemoto N, Shida Y, Shimada H, Oshima T, Yamagishi A (2003) Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum. Extremophiles 7:235–243

    PubMed  CAS  Google Scholar 

  • Niederberger TD, Götz DK, McDonald IR, Ronimus RS, Morgan HW (2006) Ignisphaera aggregans gen nov., sp. nov., a novel hyperthermophilic crenarchaeote isolated from hot springs in Rotorua and Tokaanu, New Zealand. Int J Syst Evol Microbiol 56:965–971

    Article  PubMed  CAS  Google Scholar 

  • Pancost RD, Hopmans EC, Damsté JSS et al (2001) The MEDINAUT shipboard scientific party. Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation. Geochim Cosmochim Acta 65:1611–1627

    Article  CAS  Google Scholar 

  • Park B-J, Park S-J, Yoon D-N, Schouten S, Damsté JSS, Rhee S-K (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulphur-oxidizing bacteria. Appl Environ Microbiol 76:7575–7587

    Article  PubMed  CAS  Google Scholar 

  • Pitcher A, Rychlik N, Hopmans EC, Spieck E, Rijpstra WIC, Ossebaar J, Schouten S, Wagner M, Damsté JSS (2010) Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic Group I.1b archaeon. ISME J 4:542–552

    Article  PubMed  CAS  Google Scholar 

  • Powers LA, Werne JP, Johnson TC, Hopmans EC, Damsté JSS, Schouten S (2004) Crenarchaeotal membrane lipids in lake sediments: a new paleotemperature proxy for continental paleoclimate reconstruction? Geology 70:5229–5237

    Google Scholar 

  • Reigstad LJ, Richter A, Daims H, Ulrich T, Schwark L, Schleper C (2008) Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64:167–174

    Article  PubMed  CAS  Google Scholar 

  • Reysenbach A-L, Liu Y, Banta AB, Beveridge TJ, Kirshtein JD, Schouten S (2006) A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442:444–447

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Hopmans EC, Pancost RD, Damsté JSS (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 

  • Schouten S, Hopmans EC, Schefuß E, Damsté JSS (2002) Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures? Earth Planet Sci Lett 204:265–274

    Article  CAS  Google Scholar 

  • Schouten S, van der Meer MTJ, Hopmans EC, Rijpstra WIC, Reysenbach A-L, Ward DM, Damsté JSS (2007) Archaeal and bacterial glycerol dialkyl glycerol tetraether lipids in hot springs of Yellowstone National Park. Appl Environ Microbiol 73:6181–6191

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Hopmans EC, Baas M, Boumann H, Standfest S, Könneke M, Stahl DA, Damsté JSS (2008a) Intact membrane lipids of “Candidatus Nitrosopumilus maritimus”, a cultivated representative of the cosmopolitan mesophilic group I crenarchaeota. Appl Environ Microbiol 74:2433–2440

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Baas M, Hopmans EC, Reysenbach A-L, Damsté JSS (2008b) Tetraether membrane lipids of Candidatus “Aciduliprofundum boonei”, a cultivated obligate thermoacidophilic euryarchaeote from deep-sea hydrothermal vents. Extremophiles 12:119–124

    Article  PubMed  CAS  Google Scholar 

  • Schouten S, Baas M, Hopmans EC, Damsté JSS (2008c) An unusual isoprenoid tetraether lipid in marine and lacustrine sediments. Org Geochem 39:1033–1038

    Article  CAS  Google Scholar 

  • Shimada H, Nemoto N, Shida Y, Oshima T, Yamagishi A (2008) Effects of pH and temperature on the composition of polar lipids in Thermoplasma acidophilum HO-62. J Bacteriol 190:5404–5411

    Article  PubMed  CAS  Google Scholar 

  • Sprott GD, Meloche M, Richards JC (1991) Proportions of diether, macrocyclic diether, and tetraether lipids in Methanococcus jannaschii grown at different temperatures. J Bacteriol 173:3907–3910

    PubMed  CAS  Google Scholar 

  • Stadnitskaia A, Baas M, Ivanov MK, van Weering TCE, Damsté JSS (2003) Novel archaeal macrocyclic diether core membrane lipids in a methane-derived carbonate crust from a mud volcano in the Sorokin Trough, NE Black Sea. Archaea 1:165–173

    Article  PubMed  CAS  Google Scholar 

  • Stetter KO, Thomm M, Winter J, Wildgruber G, Huber H, Zillig W, Janécovic D, König H, Palm P, Wunderl S (1981) Methanothermus fervidus, sp. nov., a novel extremely thermophilic methanogen isolated from an Icelandic hot spring. Zbl Bakt Hyg, I Abt Orig C 2 166–178

  • Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs K-U (2004) Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry—new biomarkers for biogeochemistry and microbial ecology. Rapid Commun Mass Spectrom 18:617–628

    Article  PubMed  CAS  Google Scholar 

  • Sugai A, Uda I, Itoh YH, Itoh T (2004) The core lipid composition of the 17 strains of hyperthermophilic archaea, Thermococcales. J Oleo Sci 53:41–44

    Article  CAS  Google Scholar 

  • Thurl S, Schäfer W (1988) Lipids from the sulphur-dependent Archaebacterium Thermoproteus tenax. Biochim Biophys Acta 961:253–261

    CAS  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 Archaeobacterium. J Gen Microbiol 135:2751–2757

    CAS  Google Scholar 

  • Turich C, Freeman KH, Bruns MA, Conte M, Jones AD, Wakeham SG (2007) Lipids of marine archaea: patterns and provenance in the water-column and sediments. Geochim Cosmochim Acta 71:3272–3291

    Article  CAS  Google Scholar 

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

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Uda I, Sugai A, Itoh YH, Itoh T (2004) Variation in molecular species of core lipids from the Order Thermoplasmales strains depends on the growth temperature. J Oleo Sci 53:399–404

    Article  CAS  Google Scholar 

  • Weijers JWH, Schouten S, van der Linden M, Van Geel B, Damsté JSS (2004) Water table related variations in the abundance of intact archaeal membrane lipids in a Swedish peat bog. FEMS Microbiol Lett 239:51–56

    Article  PubMed  CAS  Google Scholar 

  • Weijers JWH, Schouten S, Hopmans EC, Geenevasen JAJ, David ORP, Coleman JM, Pancost RD, Damsté JSS (2006a) Membrane lipids of mesophilic anaerobic bacteria thriving in peats have typical archaeal traits. Environ Microbiol 8:648–657

    Article  PubMed  CAS  Google Scholar 

  • Weijers JWH, Schouten S, Spaargaren OC, Damsté JSS (2006b) Occurrence and distribution of tetraether membrane lipids in soils: implications for the use of the TEX86 proxy and the BIT index. Org Geochem 37:1680–1693

    Article  CAS  Google Scholar 

  • Weijers JWH, Panoto E, van Bleijswijk J, Schouten S, Rijpstra WIC, Balk M, Stams AJM, Damsté JSS (2009) Constraints on the biological source(s) of the orphan branched tetraether membrane lipids. Geomicrobiol J 26:402–414

    Article  CAS  Google Scholar 

  • Zeikus JG, Wolfe RS (1972) Methanobacterium thermoautotrophicus sp n., an anaerobic, autotrophic, extreme thermophile. J Bacteriol 109:707–713

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge support for this study by a scholarship from the University of York. James Chong (University of York, UK; M. thermautotrophicus) and Michael Danson (University of Bath, UK; S. solfataricus and S. shibatae) are thanked for provision of the cellular material used to tune the mass spectrometer and verify the GDGT lipid assignments in I. aggregans, respectively. Two anonymous reviewers are also thanked for their constructive comments.

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Correspondence to Brendan J. Keely.

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Communicated by A. Driessen.

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Knappy, C.S., Nunn, C.E.M., Morgan, H.W. et al. The major lipid cores of the archaeon Ignisphaera aggregans: implications for the phylogeny and biosynthesis of glycerol monoalkyl glycerol tetraether isoprenoid lipids. Extremophiles 15, 517–528 (2011). https://doi.org/10.1007/s00792-011-0382-3

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