AMP-forming acetyl coenzyme a synthetase in the outermost membrane of the hyperthermophilic crenarchaeon ignicoccus hospitalis

Journal of Bacteriology

Volumn 194, Issue 6, 2012, Pages 1572-1581

  Mayer, Florian ^a,b   Küper, Ulf ^a   Meyer, Carolin ^a   Daxer, Stefanie ^a   Müller, Volker ^b   Rachel, Reinhard ^a   Huber, Harald ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; ADENOSINE PHOSPHATE; ADENOSINE PHOSPHATE FORMING ACETYL COENZYME A SYNTHETASE; BACTERIAL ENZYME; HYDROGEN; MONOMER; OXIDOREDUCTASE; SULFUR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIBODY LABELING; ARTICLE; BACTERIAL CELL; BACTERIAL OUTER MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; IGNICOCCUS HOSPITALIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

ACETATE-COA LIGASE; ADENOSINE MONOPHOSPHATE; ARCHAEAL PROTEINS; DESULFUROCOCCACEAE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MEMBRANE PROTEINS; MICROSCOPY; MODELS, BIOLOGICAL; MOLECULAR WEIGHT; PROTEIN MULTIMERIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

CRENARCHAEOTA; IGNICOCCUS;

EID: 84857961488     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06130-11     Document Type: Article

References (71)

1. Aceti DJ, Ferry JG. 1988. Purification and characterization of acetate kinase from acetate-grown Methanosarcina thermophila. Evidence for regulation of synthesis. J. Biol. Chem. 263:15444 -15448.
2. Atteia A, et al. 2006. Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J. Biol. Chem. 281: 9909-9918.
3. Berg IA, Ramos-Vera WH, Petri A, Huber H, Fuchs G. 2010. Study of the distribution of autotrophic carbon fixation cycles in Crenarchaeota. Microbiology 156:256 -269.
4. Blum H, Beier H, Gross HJ. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93-99.
5. Bräsen C, Schönheit P. 2001. Mechanisms of acetate formation and acetate activation in halophilic archaea. Arch. Microbiol. 175:360 -368.
6. Bräsen C, Schönheit P. 2004. Regulation of acetate and acetyl-CoA converting enzymes during growth on acetate and/or glucose in the halophilic archaeon Haloarcula marismortui. FEMS Microbiol. Lett. 241:21-26.
7. Bräsen C, Schönheit P. 2004. Unusual ADP-forming acetyl-coenzyme A synthetase from the mesophilic halophilic euryarchaeon Haloarcula marismortui and from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Arch. Microbiol. 182:277-287.
8. Bräsen C, Schönheit P. 2005. AMP-forming acetyl-CoA synthetase from the extremely halophilic archaeon Haloarcula marismortui: purification, identification, and expression of the encoding gene, and phylogenetic affiliation. Extremophiles 9:355-365.
9. Bräsen C, Urbanke C, Schönheit P. 2005. A novel octameric AMPforming acetyl-CoA synthetase from the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. FEBS Lett. 579:477- 482.
10. Bräsen C, Schmidt M, Grötzinger J, Schönheit P. 2008. Reaction mechanism and structural model of ADP-forming acetyl-CoA synthetase from the hyperthermophilic archaeon Pyrococcus furiosus: evidence for a second active site histidine residue. J. Biol. Chem. 283:15409 -15418.
11. Brown TDK, Jones-Mortimer MC, Kornberg HL. 1977. The enzymic interconversion of acetate and acetyl-coenzyme A in Escherichia coli. J. Gen. Microbiol. 102:327-336.
12. Burghardt T, Näther DJ, Junglas B, Huber H, Rachel R. 2007. The dominating outer membrane protein of the hyperthermophilic archaeum Ignicoccus hospitalis: a novel pore-forming complex. Mol. Microbiol. 63: 166-176.
13. Burghardt T, et al. 2009. The interaction of Nanoarchaeum equitans with Ignicoccus hospitalis: proteins in the contact site between two cells. Biochem. Soc. Trans. 37:127-132.
14. Daxer S. 2011. Master's thesis. University of Regensburg, Regensburg, Germany.
15. Frenkel EP, Kitchens RL. 1977. Purification and properties of acetylcoenzyme A synthetase from bakers' yeast. J. Biol. Chem. 252:504 -507.
16. + involvement in Bacillus subtilis. J. Bacteriol. 188:5460 -5468.
17. Glasemacher J, Bock AK, Schmid R, Schönheit P. 1997. Purification and properties of acetyl-CoA synthetase (ADP-forming), an archaeal enzyme of acetate formation and ATP synthesis, from the hyperthermophile Pyrococcus furiosus. Eur. J. Biochem. 244:561-567.
18. Grundy FJ, Turinsky AJ, Henkin TM. 1994. Catabolite regulation of Bacillus subtilis acetate and acetoin utilization genes by CcpA. J. Bacteriol. 176:4527- 4533.
19. Gulick AM, Starai VJ, Horswill AR, Homick KM, Escalante-Semerena JC. 2003. The 1.75Å crystal structure of acetyl-CoA synthetase bound to adenosine-5'-propylphosphate and coenzyme A. Biochemistry 42:2866- 2873.
20. Hallows WC, Lee S, Denu JM. 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U. S. A. 103: 10230-10235.
21. Heinonen KJ, Lahti RJ. 1981. A new and convenient colorimetric determination of inorganic orthophosphate and its application to the assay of inorganic pyrophosphatase. Anal. Biochem. 113:313-317.
22. Huber H, et al. 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. Int. J. Syst. Evol. Microbiol. 50:2093-2100.
23. Huber H, et al. 2002. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417:63- 67.
24. Huber H, et al. 2008. A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic archaeum Ignicoccus hospitalis. Proc. Natl. Acad. Sci. U. S. A. 105:7851-7856.
25. Ingram-Smith C, Smith KS. 2007. AMP-forming acetyl-CoA synthetases in Archaea show unexpected diversity in substrate utilization. Archaea 2:95-107.
26. Ingram-Smith C, Martin SR, Smith KS. 2006. Acetate kinase: not just a bacterial enzyme. Trends Microbiol. 14:249 -253.
27. Ingram-Smith C, Woods BI, Smith KS. 2006. Characterization of the acyl substrate binding pocket of acetyl-CoA synthetase, Biochemistry 45: 11482-11490.
28. Jahn U, Summons R, Sturt H, Grosjean E, Huber H. 2004. Composition of the lipids of Nanoarchaeum equitans and their origin from its host Ignicoccus sp. strain KIN4/I. Arch. Microbiol. 182:404-413.
29. 2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism. J. Bacteriol. 189:4108-4119.
30. Jahn U, et al. 2008. Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two Archaea. J. Bacteriol. 190:1743-1750.
31. Jetten MS, Stams AJ, Zehnder AJ. 1989. Isolation and characterization of acetyl-coenzyme A synthetase from Methanothrix soehngenii. J. Bacteriol. 171:5430 -5435.
32. Jetten MS, Stams AJ, Zehnder AJ. 1992. Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol. Rev. 88:181-198.
33. Jogl G, Tong L. 2004. Crystal structure of yeast acetyl-coenzyme A synthetase in complex with AMP. Biochemistry 43:1425-1431.
34. Junglas B, et al. 2008. Ignicoccus hospitalis and Nanoarchaeum equitans: ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190:395- 408.
35. Koenig T, et al. 2008. Robust prediction of the MASCOT score for an improved quality assessment in mass spectrometric proteomics. J. Proteome Res. 7:3708 -3717.
36. Kumari S, Tishel R, Eisenbach M, Wolfe AJ. 1995. Cloning, characterization, and functional expression of acs, the gene which encodes acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 177:2878 -2886.
37. Kumari S, et al. 2000. Regulation of acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 182:4173- 4179.
38. Küper U, Meyer C, Müller V, Rachel R, Huber H. 2010. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic archaeon Ignicoccus hospitalis. Proc. Natl. Acad. Sci. U. S. A. 107:3152-3156.
39. 2 via a modified Embden-Meyerhof pathway and acetyl-CoA synthetase (ADP-forming). Arch. Microbiol. 176:329- 338.
40. Martinez-Blanco H, et al. 1992. Isolation and characterization of the acetyl-CoA synthetase from Penicillium chrysogenum: involvement of this enzyme in the biosynthesis of penicillins. J. Biol. Chem. 267:5474 -5481.
41. McInerney MJ, et al. 2007. The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc. Natl. Acad. Sci. U. S. A. 104:7600 -7605.
42. Musfeldt M, Selig M, Schönheit P. 1999. Acetyl coenzyme A synthetase (ADP forming) from the hyperthermophilic archaeon Pyrococcus furiosus: identification, cloning, separate expression of the encoding genes, acdAI and acdBI, in Escherichia coli, and in vitro reconstitution of the active heterotetrameric enzyme from its recombinant subunits. J. Bacteriol. 181: 5885-5888.
43. Näther DJ, Rachel R. 2004. The outer membrane of the hyperthermophilic archaeon Ignicoccus: dynamics, ultrastructure, and composition. Biochem. Soc. Trans. 32:199 -203.
44. Neuhoff V, Arold N, Taube D, Ehrhardt W. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255-262.
45. Paper W, et al. 2007. Ignicoccus hospitalis sp. nov., the host of 'Nanoarchaeum equitans.' Int. J. Syst. Evol. Microbiol. 57:803- 808.
46. Perkins DN, Pappin DJC, Creasy DM, Cottrell JS. 1999. Probabilitybased protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567.
47. Podar M, et al. 2008. A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol. 9:R158.
48. Rachel R, Wyschkony I, Riehl S, Huber H. 2002. The ultrastructure of Ignicoccus: evidence for a novel outer membrane and for intracellular vesicle budding in an archaeon. Archaea 1:9 -18.
49. Reinscheid DJ, et al. 1999. Cloning, sequence analysis, expression and inactivation of the Corynebacterium glutamicum pta-ack operon encoding phosphotransacetylase and acetate kinase. Microbiology 145:503-513.
50. Reeves RE, Warren LG, Susskind B, Lo HS. 1977. An energy-conserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. J. Biol. Chem. 252:726 -731.
51. Reger AS, Carney JM, Gulick AM. 2007. Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochem. 46:6536-6546.
52. Rieger G, Müller K, Hermann R, Stetter KO, Rachel R. 1997. Cultivation of hyperthermophilic Archaea in capillary tubes resulting in improved preservation of fine structures. Arch. Microbiol. 168:373-379.
53. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725- 738.
54. Sanchez LB, Müller M. 1996. Purification and characterization of the acetate forming enzyme, acetyl-CoA synthetase (ADP-forming) from the amitochondriate protist, Giardia lamblia. FEBS Lett. 378:240 -244.
55. Schäfer T, Schönheit P. 1991. Pyruvate metabolism of the hyperthermophilic archaebacterium Pyrococcus furiosus: acetate formation from acetyl-CoA and ATP synthesis are catalyzed by an acetyl-CoA synthetase (ADPforming). Arch. Microbiol. 155:366 -377.
56. Schäfer T, Selig M, Schönheit P. 1993. Acetyl-CoA synthetase (ADPforming) in Archaea, a novel enzyme involved in acetate and ATP synthesis. Arch. Microbiol. 159:72- 83.
57. Schägger H. 2006. Tricine-SDS-PAGE. Nat. Protoc. 1:16 -22.
58. Schägger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:223-231.
59. Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E. 2006. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U. S. A. 103: 10224-10229.
60. Shima S, et al. 1998. Lyotropic-salt-induced changes in monomer/dimer/tetramer association equilibrium of formyltransferase from the hyperthermophilic Methanopyrus kandleri in relation to the activity and thermostability of the enzyme. Eur. J. Biochem. 258:85-92.
61. Shima S, et al. 2000. A mutation affecting the association equilibrium of formyltransferase from the hyperthermophilic Methanopyrus kandleri and its influence on the enzyme's activity and thermostability. Eur. J. Biochem. 267:6619-6623.
62. Starai VJ, Escalante-Semerena JC. 2004. Acetyl-coenzyme A synthetase (AMP forming). Cell. Mol. Life Sci. 61:2020 -2030.
63. Starai VJ, Escalante-Semerena JC. 2004. Identification of the protein acetyl-transferase (pat) enzyme that acetylates acetyl-CoA synthetases in Salmonella enterica. J. Mol. Biol. 340:1005-1012.
64. Starai VJ, Celic I, Cole RN, Boeke JD, Escalante-Semerena JC. 2002. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298:2390 -2392.
65. Starai VJ, Takahashi H, Boeke JD, Escalante-Semerena JC. 2003. Shortchain fatty acid activation by acyl-coenzyme A synthetases requires SIR2 protein function in Salmonella enterica and Saccharomyces cerevisiae. Genetics 163:545-555.
66. Sterner R, Liebl W. 2001. Thermophilic adaptation of proteins. Crit. Rev. Biochem. Mol. Biol. 36:39 -106.
67. Tauchert K, Jahn A, Oelze J. 1990. Control of diauxic growth of Azotobacter vinelandii on acetate and glucose. J. Bacteriol. 172:6447- 6451.
68. Wittig I, Braun HP, Schägger H. 2006. Blue native PAGE. Nat. Protoc. 1:418-428.
69. Wittig I, Karas M, Schägger H. 2007. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell Proteomics 6:1215-1225.
70. Wolfe AJ. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50.
71. Zeiher CA, Randall DD. 1991. Spinach leaf acetyl-coenzyme A synthetase: purification and characterization. Plant Physiol. 96:382-389.