A re-evaluation of the archaeal membrane lipid biosynthetic pathway

Nature Reviews Microbiology

Volumn 12, Issue 6, 2014, Pages 438-448

  Villanueva, Laura ^a   Damsté, Jaap S Sinninghe ^a   Schouten, Stefan ^a  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DIGERANYLGERANYLGLYCERYL PHOSPHATE; FARNESYL TRANS TRANSFERASE; GERANYLGERANYLGLYCERYL PHOSPHATE; ISOPRENYL DIPHOSPHATE SYNTHASE; MEMBRANE LIPID; MICROBIAL ENZYME; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ARCHAEON; ARTICLE; BIOCHEMISTRY; EURYARCHAEOTA; HALOBACTERIALES; LIPID BILAYER; LIPOGENESIS; NONHUMAN; PRIORITY JOURNAL; THERMOPLASMATALES; BIOSYNTHESIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

ARCHAEA;

AMINO ACID SEQUENCE; ARCHAEA; ARCHAEAL PROTEINS; CELL MEMBRANE; GENE EXPRESSION REGULATION, ARCHAEAL; MEMBRANE LIPIDS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE;

EID: 84901190009     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3260     Document Type: Article

References (58)

1. Woese, C. R. &Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088-5090 (1977).
2. Koga, Y. &Morii, H. Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol. Mol. Biol. Rev. 71, 97-120 (2007).
3. Kates, M. Biology of halophilic bacteria, Part, II. Membrane lipids of extreme halophiles: biosynthesis, function and evolutionary significance. Experientia 49, 1027-1036 (1993).
4. Thompson, D. H. et al. Tetraether bolaform amphiphiles as models of archae-bacterial membrane lipids: Raman spectroscopy, 31P NMR, X-ray scattering, and electron microscopy. J. Am. Chem. Soc. 114, 9035-9042 (1992).
5. Sinninghe Damsté, J. S., Hopmans, E. C., Schouten, S., van Duin, A. C. T. &Geenevasen, J. A. J. Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J. Lipid Res. 43, 1641-1651 (2002).
6. Jarrell, K. F. et al. Major players on the microbial stage: why archaea are important. Microbiology 157, 919-936 (2011).
7. Wuchter, C. et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317-12322 (2006).
8. Boucher, Y., Kamekura, M. &Doolittle, W. F. Origins and evolution of isoprenoid lipid biosynthesis in archaea. Mol. Microbiol. 52, 515-527 (2004).
9. Lombard, J., Lopez-Garcia, P. &Moreira, D. Phylogenomic investigation of phospholipid synthesis on archaea. Archaea 2012, 630910 (2012).
10. Schouten, S., Hopmans, E. C. &Sinninghe Damsté, J. S. The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: a review. Org. Geochem. 54, 19-61 (2013).
11. 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).
12. Gribaldo, S. &Brochier-Armanet, C. The origin and evolution of Archaea: a state of the art. Phil. Trans. R. Soc. B 361, 1007-1022 (2006).
13. Stetter, K. O., Fiala, G., Huber, G., Huber, R. &Segerer, A. Hyperthemophilic microorganisms. FEMS Microbiol. Rev. 75, 117-124 (1990).
14. Madsen, E. L. Environmental Microbiology: From Genomes to Biogeochemistry. (Wiley-Blackwell, 2008).
15. Nelson-Sathi, S. et al. Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl Acad. Sci. USA http://dx.doi.org/10.1073/pnas.1209119109 (2012).
16. Ruepp, A. et al. The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407, 508-5139 (2000).
17. Brochier-Armanet, C., Forterre, P. &Gribaldo, S. Phylogeny and evolution of the Archaea: one hundred genomes later. Curr. Opin. Microbiol. 14, 274-281 (2011).
18. Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102-8107 (2008).
19. Huber, H., Hohn, M. J., Stetter, K. O. &Rachel, R. The phylum Nanoarchaeota: present knowledge and future perspectives of a unique form of life. Res. Microbiol. 154, 165-171 (2003).
20. Brochier-Armanet, C., Boussau, B., Gribaldo, S. &Forterre, P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Rev. Microbiol. 6, 245-252 (2008).
21. Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204-3223 (2011).
22. Pester, M., Schleper, C. &Wagner, M. The Thaumarchaeota: An emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300-306 (2011).
23. Koga, Y. &Morii, H. Recent advances in structural research on ether lipids from Archaea including comparative and physiological aspects. Biosci. Biotechnol. Biochem. 69, 2019-2034 (2005).
24. Koga, Y., Akagawa-Matsushita, M., Ohga, M. &Nishihara, M. Taxonomic significance of the distribution of component parts of polar ether lipids in methanogens. Syst. Appl. Microbiol. 16, 342-351 (1993).
25. Langworthy, T. A. in The Bacteria (eds Woese, C. R. &Wolfe, R. S.) 459-497 (Academic Press,1985).
26. Uda, I., Sugai, A., Itoh, Y. H. &Itoh, T. Variation in molecular species of polar lipids from Thermoplasma acidophilum depends on growth temperature. Lipids 36, 103-105 (2001).
27. Chong, P. L. G. Archaebacterial bipolar tetraether lipids: physico-chemical and membrane properties. Chem. Phys. Lip. 163, 253-265 (2010).
28. Macalady, J. L. et al. Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 8, 411-419 (2004).
29. Pitcher, A. et al. Core and intact polar glycerol dibiphytanyl glycerol tetraether lipids of ammonia-oxidizing archaea enriched from marine and estuarine sediments. Appl. Environ. Microbiol. 77, 3468-3477 (2011).
30. Reysenbach, A. L. et al. Isolation of a ubiquitous obligate thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444-447 (2006).
31. De Rosa, M. et al. An asymmetric archaebacterial diether lipid from alkaliphilic halophiles. J. Gen. Microbiol. 128, 343-348 (1982).
32. Matsumi, R., Atomi, H., Driessen, A. J. &van der Oost, J. Isoprenoid biosynthesis in archaea-biochemical and evolutionary implications. Res. Microbiol. 162, 39-52 (2011).
33. Lai, D. Isoprenoid Ether Lipid Biosynthesis in the Extremophile, Archaeoglobus fulgidus. Thesis, Univ. California Los Angeles (2009).
34. Langworthy, T. A. Turnover of di-O-phytanylglycerol in Thermoplasma. Rev. Infect. Dis. 4, S266 (1982).
35. Nemoto, N., Shida, Y., Shimada, H., Oshima, T. &Yamagishi, A. Characterization of the precursor of tetraether lipid biosynthesis in the thermoacidophilic archaeon Thermoplasma acidophilum. Extremophiles 7, 235-243 (2003).
36. Poulter, C. D., Aoki, T. &Daniels, L. Biosynthesis of isoprenoid membranes in the methanogenic archaebacterium Methanospirillum hungatei. J. Am. Chem. Soc. 110, 2620-2624 (1988).
37. Eguchi, T., Takyo, H., Morita, M., Kakinuma, K. &Koga, Y. Unusual double-bond migration as plausible key reaction on the synthesis of the isoprenoid membrane lipids of methanogenic archaea. J. Chem. Soc. Chem. Commun. 2000, 1545-1546 (2000).
38. Eguchi, T. Nishimura, Y. &Kakinuma, K. Importance of the isopropylene terminal of geranylgeranyl group for the formation of tetraether lipid in methanogenic archaea. Tetrahedron Lett. 44, 3275-3279 (2003).
39. Wang, K. C. &Ohnuma, S. I. Isoprenyl diphosphate synthases. Biochim. Biophys. Acta. 1529, 33-48 (2000).
40. Wang, K. &Ohnuma, S. Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. Trends Biochem. Sci. 24, 445-451 (1999).
41. Chen, A. &Poulter, C. D. Purification and characterization of farnesyl diphosphate/geranylgeranyl diphosphate synthase. A thermostable bifunctional enzyme from Methanobacterium thermoautotrophicum. J. Biol. Chem. 268, 11002-11007 (1993).
42. Ogawa, T., Yoshimura, T. &Hemmi, H. Geranylfarnesyl diphosphate synthase from Methanosarcina mazei: different role, different evolution. Biochem. Biophys. Res. Commun. 393, 16e20 (2010).
43. Peters, K. E., Wlaters, C. C. &Moldowan, J. M. The biomarker guide: Biomarkers and Isotopes in Petroleum Exploration and Earth History 2nd edn (Cambridge University Press, 2007).
44. Zhang, D. &Poulter, C. D. Biosynthesis of archaebacterial ether lipids. Formation of ether linkages by prenyltransferases. J. Am. Chem. Soc. 115, 1270-1277 (1993).
45. Payadeh, J., Fujihashi, M., Gillon, W. &Pai, E. F. The crystal structure of (S)-3-O-geranylgeranylglyceryl phosphate synthase reveals an ancient fold for an ancient enzyme. J. Biol. Chem. 281, 6070-6078 (2006).
46. Guldan, H., Matysik, F. M., Bocola, M., Sterner, R. &Babinger, P. Functional assignment of an enzyme that catalyzes the synthesis of an Archaea-type ether lipid in Bacteria. Angew. Chem. Int. Ed. 50, 8188-8191 (2011).
47. Ren, F. et al. Insights into TIM-barrel prenyl transferase mechanisms: crystal structures of PcrB from Bacillus subtilis and Staphylococcus aureus. ChemBioChem. 14, 195-199 (2013).
48. Hemmi, H., Shibuya, K., Takahashi, Y., Nakayama, T. &Nishino, T. J. (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. Biol. Chem. 279, 50197-50203 (2004).
49. Klassen, J. L. Phylogenetic and evolutionary patterns in microbial carotenoid biosynthesis are revealed by comparative genomics. PLoS ONE 5, e11257 (2010).
50. Knappy, C. S. &Keely, B. J. Novel glycerol dialkanol triols in sediments: transformation products of glycerol diphytanyl glycerol tetraether lipids or biosynthetic intermediates? Chem. Commun. 48, 841-843 (2012).
51. Liu, X. -L., Lipp, J. S., Schröder, J. M., Summons, R. E. &Hinrichs, K. -U. Isoprenoid glycerol dialkanol diethers: a series of novel archaeal lipids in marine sediments. Org. Geochem. 43, 50-55 (2012).
52. Schouten, S., Hoefs, M. J. L., Koopmans, M. P., Bosch, H. J. &Sinninghe Damsté, J. S. Structural characterization, ocurrence and fate of archaeal ether-bound acyclic and cyclic biphytanes and corresponding diols in sediments. Org. Geochem. 29, 1305-1319 (1998).
53. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
54. Cole, C., Barber, J. D. &Barton, G. J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 35, W197-W201 (2008).
55. Talavera, G. &Castresana, J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564-577 (2007).
56. Abascal, F., Zardoya, R. &Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 (2005).
57. Letunic, I. &Bork, P. Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128 (2007).
58. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010).