Phylogenomic reconstruction of archaeal fatty acid metabolism

Environmental Microbiology

Volumn 16, Issue 4, 2014, Pages 907-918

  Dibrova, Daria V ^a,b   Galperin, Michael Y ^c   Mulkidjanian, Armen Y ^a,b  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS);

3 HYDROXYACYL COENZYME A DEHYDROGENASE; ACYL COENZYME A DEHYDROGENASE; ENOYL COENZYME A HYDRATASE; FATTY ACID; MULTIENZYME COMPLEX;

ARCHAEON; ARTICLE; GENETICS; GENOMICS; HORIZONTAL GENE TRANSFER; METABOLISM; OXIDATION REDUCTION REACTION; PHYLOGENY;

3-HYDROXYACYL COA DEHYDROGENASES; ACYL-COA DEHYDROGENASE; ARCHAEA; ENOYL-COA HYDRATASE; FATTY ACIDS; GENE TRANSFER, HORIZONTAL; GENOMICS; MULTIENZYME COMPLEXES; OXIDATION-REDUCTION; PHYLOGENY;

EID: 84898058598     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12359     Document Type: Article

References (73)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zheng, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST - a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Benner, S.A., Ellington, A.D., and Tauer, A. (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci U S A 86: 7054-7058.
3. Boucher, Y., Kamekura, M., and Doolittle, W.F. (2004) Origins and evolution of isoprenoid lipid biosynthesis in archaea. Mol Microbiol 52: 515-527.
4. Carballeira, N.M., Reyes, M., Sostre, A., Huang, H., Verhagen, M.F., and Adams, M.W. (1997) Unusual fatty acid compositions of the hyperthermophilic archaeon Pyrococcus furiosus and the bacterium Thermotoga maritima. J Bacteriol 179: 2766-2768.
5. Caspi, R., Altman, T., Dreher, K., Fulcher, C.A., Subhraveti, P., Keseler, I.M., etal. (2012) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 40: D742-D753.
6. Clomburg, J.M., Vick, J.E., Blankschien, M.D., Rodríguez-Moyá, M., and Gonzalez, R. (2012) A synthetic biology approach to engineer a functional reversal of the β-oxidation cycle. ACS Synth Biol 1: 541-554.
7. Corcelli, A., and Lobasso, S. (2006) Characterization of lipids of halophilic Archaea. In Methods in Microbiology, Extremophiles. Rainey, F.A., and Oren, A. (eds). London, UK: Academic Press, pp. 585-613.
8. Corcelli, A., Lobasso, S., Colella, M., Trotta, M., Guerrieri, A., and Palmisano, F. (1996) Role of palmitic acid on the isolation and properties of halorhodopsin. Biochim Biophys Acta 1281: 173-181.
9. Dellomonaco, C., Clomburg, J.M., Miller, E.N., and Gonzalez, R. (2011) Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 476: 355-359.
10. Dibrova, D.V. (2013) Phylogenomic analysis of energy converting enzymes. PhD thesis. Universität Osnabrück, Osnabrück, 259 pp.
11. Dibrova, D.V., Chudetsky, M.Y., Galperin, M.Y., Koonin, E.V., and Mulkidjanian, A.Y. (2012) Role of energy in the emergence of biology from chemistry. Orig Life Evol Biosph 42: 459-468.
12. Dibrova, D.V., Cherepanov, D.A., Galperin, M.Y., Skulachev, V.P., and Mulkidjanian, A.Y. (2013) Evolution of cytochrome bc complexes: from membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates. Biochim Biophys Acta 1827: 1407-1427.
13. Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
14. 13C nuclear magnetic resonance study. J Bacteriol 166: 559-564.
15. Falb, M., Muller, K., Konigsmaier, L., Oberwinkler, T., Horn, P., von Gronau, S., etal. (2008) Metabolism of halophilic archaea. Extremophiles 12: 177-196.
16. Fukui, T., Shiomi, N., and Doi, Y. (1998) Expression and characterization of (R)-specific enoyl coenzyme A hydratase involved in polyhydroxyalkanoate biosynthesis by Aeromonas caviae. J Bacteriol 180: 667-673.
17. Gattinger, A., Schloter, M., and Munch, J.C. (2002) Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling. FEMS Microbiol Lett 213: 133-139.
18. Gochnauer, M.B., and Kushner, D.J. (1969) Growth and nutrition of extremely halophilic bacteria. Can J Microbiol 15: 1157-1165.
19. 1. Biochemistry 38: 9031-9038.
20. Gonzalez, O. (2009) Reconstruction, modeling & analysis of haloarchaeal metabolic networks. PhD thesis, Ludwig-Maximilians-Universität, München, 202 pp.
21. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
22. Hasan, S.S., Yamashita, E., Ryan, C.M., Whitelegge, J.P., and Cramer, W.A. (2011) Conservation of lipid functions in cytochrome bc complexes. J Mol Biol 414: 145-162.
23. Heider, J. (2001) A new family of CoA-transferases. FEBS Lett 509: 345-349.
24. Helgersons, S., Siemsens, S., and Dratz, E. (1992) Enrichment of bacteriorhodopsin with isotopically labeled amino acids by biosynthetic incorporation in Halobacterium halobium. Can J Microbiol 38: 1181-1185.
25. Hemp, J., and Gennis, R.B. (2008) Diversity of the heme-copper superfamily in archaea: Insights from genomics and structural modeling. In Results and Problems in Cell Differentiation. Schäfer, G., and Penefsky, H.S. (eds). Berlin: Springer-Verlag, pp. 1-31.
26. Hemp, J., Laura, A.P., and Gennis, R.B. (2012) The heme-copper oxidoreductase superfamily: diversity, evolution and ecology. Biochim Biophys Acta 1817: S107-S108.
27. Jiang, C., Kim, S.Y., and Suh, D.Y. (2008) Divergent evolution of the thiolase superfamily and chalcone synthase family. Mol Phylogenet Evol 49: 691-701.
28. Kashefi, K., Tor, J.M., Holmes, D.E., Gaw Van Praagh, C.V., Reysenbach, A.-L., and Lovley, D.R. (2002) Geoglobus ahangari gen. nov., sp. nov., a novel hyperthermophilic archaeon capable of oxidizing organic acids and growing autotrophically on hydrogen with Fe(III) serving as the sole electron acceptor. Int J Syst Evol Microbiol 52: 719-728.
29. Khelifi, N., Grossi, V., Hamdi, M., Dolla, A., Tholozan, J.L., Ollivier, B., and Hirschler-Rea, A. (2010) Anaerobic oxidation of fatty acids and alkenes by the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus. Appl Environ Microbiol 76: 3057-3060.
30. Koga, Y., and Morii, H. (2007) Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71: 97-120.
31. Koga, Y., Nishihara, M., Morii, H., and Akagawa-Matsushita, M. (1993) Ether polar lipids of methanogenic bacteria: structures, comparative aspects, and biosyntheses. Microbiol Rev 57: 164-182.
32. Koga, Y., Kyuragi, T., Nishihara, M., and 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.
33. Kolbe, M., Besir, H., Essen, L.O., and Oesterhelt, D. (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 A resolution. Science 288: 1390-1396.
34. Koonin, E.V., and Galperin, M.Y. (2003) Sequence - Evolution - Function. Computational Approaches in Comparative Genomics. Boston: Kluwer Academic.
35. 2 by mitochondria in the resting state. FEBS Lett 435: 215-218.
36. Kuznetsova, E., Proudfoot, M., Sanders, S.A., Reinking, J., Savchenko, A., Arrowsmith, C.H., etal. (2005) Enzyme genomics: application of general enzymatic screens to discover new enzymes. FEMS Microbiol Rev 29: 263-279.
37. Leuko, S., Raftery, M.J., Burns, B.P., Walter, M.R., and Neilan, B.A. (2009) Global protein-level responses of Halobacterium salinarum NRC-1 to prolonged changes in external sodium chloride concentrations. J Proteome Res 8: 2218-2225.
38. Lobasso, S., Lopalco, P., Angelini, R., Vitale, R., Huber, H., Muller, V., and Corcelli, A. (2012) Coupled TLC and MALDI-TOF/MS analyses of the lipid extract of the hyperthermophilic archaeon Pyrococcus furiosus. Archaea 2012: 957852.
39. Lombard, J., Lopez-Garcia, P., and Moreira, D. (2012a) An ACP-independent fatty acid synthesis pathway in archaea: implications for the origin of phospholipids. Mol Biol Evol 29: 3261-3265.
40. Lombard, J., Lopez-Garcia, P., and Moreira, D. (2012b) The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10: 507-515.
41. Lombard, J., Lopez-Garcia, P., and Moreira, D. (2012c) Phylogenomic investigation of phospholipid synthesis in archaea. Archaea 2012: 630910.
42. Maier, T., Leibundgut, M., and Ban, N. (2008) The crystal structure of a mammalian fatty acid synthase. Science 321: 1315-1322.
43. Makarova, K.S., Aravind, L., Galperin, M.Y., Grishin, N.V., Tatusov, R.L., Wolf, Y.I., and Koonin, E.V. (1999) Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. Genome Res 9: 608-628.
44. Makarova, K.S., Sorokin, A.V., Novichkov, P.S., Wolf, Y.I., and Koonin, E.V. (2007) Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea. Biol Direct 2: 33.
45. Miziorko, H.M. (2011) Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch Biochem Biophys 505: 131-143.
46. Muh, U., Cinkaya, I., Albracht, S.P., and Buckel, W. (1996) 4-Hydroxybutyryl-CoA dehydratase from Clostridium aminobutyricum: characterization of FAD and iron-sulfur clusters involved in an overall non-redox reaction. Biochemistry 35: 11710-11718.
47. Mulkidjanian, A.Y., and Galperin, M.Y. (2010) Evolutionary origins of membrane proteins. In Structural Bioinformatics of Membrane Proteins. Frishman, D. (ed.). Vienna: Springer, pp. 1-28.
48. Mulkidjanian, A.Y., Galperin, M.Y., Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2008) Evolutionary primacy of sodium bioenergetics. Biol Direct 3: 13.
49. Mulkidjanian, A.Y., Galperin, M.Y., and Koonin, E.V. (2009) Co-evolution of primordial membranes and membrane proteins. Trends Biochem Sci 34: 206-215.
50. Nakaya, A., Katayama, T., Itoh, M., Hiranuka, K., Kawashima, S., Moriya, Y., etal. (2013) KEGG OC: a large-scale automatic construction of taxonomy-based ortholog clusters. Nucleic Acids Res 41: D353-D357.
51. Nelson-Sathi, S., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J.O., etal. (2012) Acquisition of 1000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci U S A 109: 20537-20542.
52. Nicholas, K.B., Nicholas, H.B., Jr, and Deerfield, D.W., II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4: 14.
53. Nishihara, M., Nagahama, S., Ohga, M., and Koga, Y. (2000) Straight-chain fatty alcohols in the hyperthermophilic archaeon Pyrococcus furiosus. Extremophiles 4: 275-277.
54. Oesterhelt, D., and Krippahl, G. (1973) Light inhibition of respiration in Halobacterium halobium. FEBS Lett 36: 72-76.
55. Pereto, J., Lopez-Garcia, P., and Moreira, D. (2005) Phylogenetic analysis of eukaryotic thiolases suggests multiple proteobacterial origins. J Mol Evol 61: 65-74.
56. Powell, S., Szklarczyk, D., Trachana, K., Roth, A., Kuhn, M., Muller, J., etal. (2012) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40: D284-D289.
57. Pruitt, K.D., Tatusova, T., Brown, G.R., and Maglott, D.R. (2012) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 40: D130-D135.
58. Pugh, E.L., and Kates, M. (1994) Acylation of proteins of the archaebacteria Halobacterium cutirubrum and Methanobacterium thermoautotrophicum. Biochim Biophys Acta 1196: 38-44.
59. Pugh, E.L., Wassef, M.K., and Kates, M. (1971) Inhibition of fatty acid synthetase in Halobacterium cutirubrum and Escherichia coli by high salt concentrations. Can J Biochem 49: 953-958.
60. Rock, C.O., and Cronan, J.E. (1996) Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim Biophys Acta 1302: 1-16.
61. Rock, C.O., and Jackowski, S. (2002) Forty years of bacterial fatty acid synthesis. Biochem Biophys Res Commun 292: 1155-1166.
62. Sanchez, L.B., Galperin, M.Y., and Müller, M. (2000) Acetyl-CoA synthetase from the amitochondriate eukaryote Giardia lamblia belongs to the newly recognized superfamily of acyl-CoA synthetases (nucleoside diphosphate-forming). J Biol Chem 275: 5794-5803.
63. 2 digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry 38: 14966-14972.
64. Shinzawa-Itoh, K., Aoyama, H., Muramoto, K., Terada, H., Kurauchi, T., Tadehara, Y., etal. (2007) Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26: 1713-1725.
65. Slobodkina, G.B., Kolganova, T.V., Querellou, J., Bonch-Osmolovskaya, E.A., and Slobodkin, A.I. (2009) Geoglobus acetivorans sp. nov., an iron(III)-reducing archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 59: 2880-2883.
66. Smit, A., and Mushegian, A. (2000) Biosynthesis of isoprenoids via mevalonate in Archaea: the lost pathway. Genome Res 10: 1468-1484.
67. Smith, S. (1994) The animal fatty acid synthase: one gene, one polypeptide, seven enzymes. FASEB J 8: 1248-1259.
68. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
69. Tatusov, R.L., Koonin, E.V., and Lipman, D.J. (1997) A genomic perspective on protein families. Science 278: 631-637.
70. Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V. (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28: 33-36.
71. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., etal. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
72. Wolf, Y.I., Makarova, K.S., Yutin, N., and Koonin, E.V. (2012) Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer. Biol Direct 7: 46.
73. Worm, P., Muller, N., Plugge, C.M., Stams, A.J.M., and Schink, B. (2010) Syntrophy in Methanogenic Degradation. In Microbiology Monographs: (Endo)symbiotic Methanogenic Archaea. Hackstein, J.H.P. (ed.). Berlin: Springer-Verlag, pp. 143-173.