Conserved P-loop GTPases of unknown function in bacteria: An emerging and vital ensemble in bacterial physiology

Biochemistry and Cell Biology

Volumn 83, Issue 6, 2005, Pages 738-746

  Brown, Eric D ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Essential gene; GTPase; P loop; Unknown function

Indexed keywords

BACTERIA; CHARACTERIZATION; GENES; PHYSIOLOGY; PROTEINS; RNA;

ESSENTIAL GENES; GTPASE; P-LOOP; UNKNOWN FUNCTION;

ENZYME KINETICS;

ADENOSINE TRIPHOSPHATASE; GENE PRODUCT; GUANOSINE TRIPHOSPHATASE; TRANSFER RNA;

CATALYSIS; CELL FUNCTION; CONFERENCE PAPER; ESSENTIAL GENE; GENE FUNCTION; PHENOTYPE; PLEIOTROPY; PROTEIN DOMAIN; RIBOSOME;

BACTERIA; BACTERIAL PHYSIOLOGY; GTP PHOSPHOHYDROLASES; PROTEIN BIOSYNTHESIS; RIBOSOMES;

BACTERIA (MICROORGANISMS);

EID: 32044468906     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o05-162     Document Type: Conference Paper

References (90)

1. Ahnn, J., March, P.E., Takiff, H.E., and Inouye, M. 1986. A GTP-binding protein of Escherichia coli has homology to yeast RAS proteins. Proc. Natl. Acad. Sci. U.S.A. 83(23): 8849-8853.
2. Alam, K. Y. and Clark, D.P. 1991. Molecular cloning and sequence of the thdF gene, which is involved in thiophene and furan oxidation by Escherichia coli. J. Bacteriol. 173(19): 6018-6024.
3. Allali-Hassani, A., Campbell, T.L., Ho, A., Schertzer, J.W., and Brown, E.D. 2004. Probing the active site of YjeE: a vital Escherichia coli protein of unknown function. Biochem. J. 384(Pt 3): 577-584.
4. Arigoni, F., Talabot, F., Peitsch, M., Edgerton, M.D., Meldrum, E., Allet, E. et al. 1998. A genome-based approach for the identification of essential bacterial genes. Nat. Biotechnol. 16(9): 851-856.
5. Bourne, H.R., Sanders, D.A., and McCormick, F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature (London), 349(6305): 117-127.
6. Brierley, I., Meredith, M.R., Bloys, A.J., and Hagervall, T.G. 1997. Expression of a coronavirus ribosomal frameshift signal in Escherichia coli: influence of tRNA anticodon modification on frameshifting. J. Mol. Biol. 270(3): 360-373.
7. Britton, R.A., Powell, B.S., Court, D.L., and Lupski, J.R. 1997. Characterization of mutations affecting the Escherichia coli essential GTPase era that suppress two temperature-sensitive dnaG alleles. J. Bacteriol. 179(14): 4575-4582.
8. Britton, R.A., Powell, B.S., Dasgupta, S., Sun, Q., Margolin, W., Lupski, J.R., and Court, D.L. 1998. Cell cycle arrest in Era GTPase mutants: a potential growth rate-regulated checkpoint in Escherichia coli. Mol. Microbiol. 27(4): 739-750.
9. Buglino, J., Shen, V. Hakimian, P., and Lima, C.D. 2002. Structural and biochemical analysis of the Obg GTP binding protein. Structure (Cambridge), 10(11): 1581-1592.
10. Cabedo, H., Macian, F., Villarroya, M., Escudero, J.C., Martinez-Vicente, M., Knecht, E., and Armengod, M.E. 1999. The Escherichia coli trmE (mnmE) gene, involved in tRNA modification, codes for an evolutionarily conserved GTPase with unusual biochemical properties. EMBO J. 18(24): 7063-7076.
11. Caldon, C.E., and March, P.E. 2003. Function of the universally conserved bacterial GTPases. Curr. Opin. Microbiol. 6(2): 135-139.
12. Caldon, C.E., Yoong, P., and March, P.E. 2001. Evolution of a molecular switch: universal bacterial GTPases regulate ribosome function. Mol. Microbiol. 41(2): 289-297.
13. Campbell, T.L., Daigle, D.M., and Brown, E.D. 2005. Characterization of the Bacillus subtilis GTPase YloQ and its role in ribosome function. Biochem. J. 389: 843-852.
14. Chen, X., Court, D.L., and Ji, X. 1999. Crystal structure of ERA: a GTPase-dependent cell cycle regulator containing an RNA binding motif. Proc. Natl. Acad. Sci. U.S.A. 96(15): 8396-8401.
15. Daigle, D.M., and Brown, E.D. 2004. Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J. Bacteriol. 186(5): 1381-1387.
16. Daigle, D.M., Rossi, L., Berghuis, A.M., Aravind, L., Koonin, E.V., and Brown, E.D. 2002. YjeQ, an essential, conserved, uncharacterized protein from Escherichia coli, is an unusual GTPase with circularly permuted G-motifs and marked burst kinetics. Biochemistry, 41(37): 11109-11117.
17. Dassain, M., Leroy, A., Colosetti, L., Carole, S., and Bouche, J.P. 1999. A new essential gene of the 'minimal genome' affecting cell division. Biochimie, 81(8-9): 889-895.
18. Datta, K., Skidmore, J.M., Pu, K., and Maddock, J.R. 2004. The Caulobacter crescentus GTPase CgtAC is required for progression through the cell cycle and for maintaining 50S ribosomal subunit levels. Mol. Microbiol. 54(5): 1379-1392.
19. Elseviers, D., Petrullo, L.A., and Gallagher, P.J. 1984. Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine. Nucleic Acids Res. 12(8): 3521-3534.
20. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R. et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science (Washington, D.C.), 269(5223): 496-512.
21. Foti, J.J., Schienda, J., Sutera, V.A., Jr., and Lovett, S.T. 2005. A bacterial G protein-mediated response to replication arrest. Mol. Cell, 17(4): 549-560.
22. Freiberg, C., Wieland, B., Spaltmann, F., Ehlert, K., Brotz, H., and Labischinski, H. 2001. Identification of novel essential Escherichia coli genes conserved among pathogenic bacteria. J. Mol. Microbiol. Biotechnol. 3(3): 483-489.
23. Galperin, M.Y., and Koonin, E.V. 2004. 'Conserved hypothetical' proteins: prioritization of targets for experimental study. Nucleic Acids Res. 32(18): 5452-5463.
24. Gerdes, S.Y., Scholle, M.D., Campbell, J.W., Balazsi, G., Ravasz, E., Daugherty, M.D. et al. 2003. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J. Bacteriol. 185(19): 5673-5684.
25. Gollop, N., and March, P.E. 1991. A GTP-binding protein (Era) has an essential role in growth rate and cell cycle control in Escherichia coli. J. Bacteriol. 173(7): 2265-2270.
26. Hagervall, T.G., Pomerantz, S.C., and McCloskey, J.A. 1998. Reduced misreading of asparagine codons by Escherichia coli tRNALys with hypomodified derivatives of 5-methylaminomethyl-2-thiouridine in the wobble position. J. Mol. Biol. 284(1): 33-42.
27. Hang, J.Q., and Zhao, G. 2003. Characterization of the 16S rRNA- and membrane-binding domains of Streptococcus pneumoniae Era GTPase: structural and functional implications. Eur. J. Biochem. 270(20): 4164-4172.
28. Hang, J.Q., Meier, T.I., and Zhao, G. 2001. Analysis of the interaction of 16S rRNA and cytoplasmic membrane with the C-terminal part of the Streptococcus pneumoniae Era GTPase. Eur. J. Biochem. 268(21): 5570-5577.
29. Himeno, H., Hanawa-Suetsugu, K., Kimura, T., Takagi, K., Sugiyama, W., Shirata, S. et al. 2004. A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res. 32(17): 5303-5309.
30. Hwang, J., and Inouye, M. 2001. An essential GTPase, der, containing double GTP-binding domains from Escherichia coli and Thermotoga maritima. J. Biol. Chem. 276(33): 31415-31421.
31. Inoue, K., Chen, J., Kato, I., and Inouye, M. 2002. Specific growth inhibition by acetate of an Escherichia coli strain expressing Era-dE, a dominant negative Era mutant. J. Mol. Microbiol. Biotechnol. 4(4): 379-388.
32. Inoue, K., Alsina, J., Chen, J., and Inouye, M. 2003. Suppression of defective ribosome assembly in a rbfA deletion mutant by overexpression of Era, an essential GTPase in Escherichia coli. Mol. Microbiol. 48(4): 1005-1016.
33. Johnstone, B.H., Handler, A.A., Chao, D.K., Nguyen, V., Smith, M., Ryu, S.Y. et al. 1999. The widely conserved Era G-protein contains an RNA-binding domain required for Era function in vivo. Mol. Microbiol. 33(6): 1118-1131.
34. Kobayashi, G., Moriya, S., and Wada, C. 2001. Deficiency of essential GTP-binding protein ObgE in Escherichia coli inhibits chromosome partition. Mol. Microbiol. 41(5): 1037-1051.
35. Kobayashi, K., Ehrlich, S.D., Albertini, A., Amati, G., Andersen, K.K., Arnaud, M. et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. U.S.A. 100(8): 4678-4683.
36. Kok, J., Trach, K.A., and Hoch, J.A. 1994. Effects on Bacillus subtilis of a conditional lethal mutation in the essential GTP-binding protein Obg. J. Bacteriol. 176(23): 7155-7160.
37. Koonin, E.V., Wolf, Y.I., and Aravind, L. 2000. Protein fold recognition using sequence profiles and its application in structural genomics. Adv. Protein Chem. 54: 245-275.
38. Kukimoto-Niino, M., Murayama, K., Inoue, M., Terada, T., Tame, J.R., Kuramitsu, S. et al. 2004. Crystal structure of the GTP-binding protein Obg from Thermus thermophilus HB8. J. Mol. Biol. 337(3): 761-770.
39. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J. et al. 2001. Initial sequencing and analysis of the human genome. Nature (London), 409(6822): 860-921.
40. Lehoux, I.E., Mazzulla, M.J., Baker, A., and Petit, C.M. 2003. Purification and characterization of YihA, an essential GTP-binding protein from Escherichia coli. Protein Expr. Purif. 30(2): 203-209.
41. Leipe, D.D., Wolf, Y.I., Koonin, E.V., and Aravind, L. 2002. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317(1): 41-72.
42. Leipe, D.D., Koonin, E.V., and Aravind, L. 2003. Evolution and classification of P-loop kinases and related proteins. J. Mol. Biol. 333(4): 781-815.
43. Lerner, C.G., and Inouye, M. 1991. Pleiotropic changes resulting from depletion of Era, an essential GTP-binding protein in Escherichia coli. Mol. Microbiol. 5(4): 951-957.
44. Levdikov, V.M., Blagova, E.V., Brannigan, J.A., Cladiere, L., Antson, A.A., Isupov, M.N. et al. 2004. The crystal structure of YloQ, a circularly permuted GTPase essential for Bacillus subtilis viability. J. Mol. Biol. 340(4): 767-782.
45. Lewis, L.M., Engle, L.J., Pierceall, W.E., Hughes, D.E., and Shaw, K.J. 2004. Affinity capillary electrophoresis for the screening of novel antimicrobial targets. J. Biomol. Screen. 9(4): 303-308.
46. Lin, B., Covalle, K.L., and Maddock, J.R. 1999. The Caulobacter crescentus CgtA protein displays unusual guanine nucleotide binding and exchange properties. J. Bacteriol. 181(18): 5825-5832.
47. Lu, Q., and Inouye, M. 1998. The gene for 16S rRNA methyl-transferase (ksgA) functions as a multicopy suppressor for a cold-sensitive mutant of era, an essential RAS-like GTP-binding protein in Escherichia coli. J. Bacteriol. 180(19): 5243-5246.
48. Maddock, J., Bhatt, A., Koch, M., and Skidmore, J. 1997. Identification of an essential Caulobacter crescentus gene encoding a member of the Obg family of GTP-binding proteins. J. Bacteriol. 179(20): 6426-6431.
49. Mehr, I.J., Long, C.D., Serkin, C.D., and Seifert, H.S. 2000. A homologue of the recombination-dependent growth gene, rdgC, is involved in gonococcal pilin antigenic variation. Genetics, 154(2): 523-532.
50. Meier, T.I., Peery, R.B., Jaskunas, S.R., and Zhao, G. 1999. 16S rRNA is bound to era of Streptococcus pneumoniae. J. Bacteriol. 181(17): 5242-5249.
51. Meier, T.I., Peery, R.B., McAllister, K.A., and Zhao, G. 2000. Era GTPase of Escherichia coli: binding to 16S rRNA and modulation of GTPase activity by RNA and carbohydrates. Microbiology, 146(Pt 5): 1071-1083.
52. Minkovsky, N., Zarimani, A., Chary, V.K., Johnstone, B.H., Powell, B.S., Torrance, P.D. et al. 2002. Bex, the Bacillus subtilis homolog of the essential Escherichia coli GTPase Era, is required for normal cell division and spore formation. J. Bacteriol. 184(22): 6389-6394.
53. Mittenhuber, G. 2001. Comparative genomics of prokaryotic GTP-binding proteins (the Era, Obg, EngA, ThdF (TrmE), YchF and YihA families) and their relationship to eukaryotic GTP-binding proteins (the DRG, ARF, RAB, RAN, RAS and RHO families). J. Mol. Microbiol. Biotechnol. 3(1): 21-35.
54. Morimoto, T., Loh, P.C., Hirai, T., Asai, K., Kobayashi, K., Moriya, S., and Ogasawara, N. 2002. Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology, 148(Pt 11): 3539-3552.
55. Natale, D.A., Galperin, M.Y., Tatusov, R.L., and Koonin, E.V. 2000. Using the COG database to improve gene recognition in complete genomes. Genetica, 108(1): 9-17.
56. Noble, J.A., Innis, M.A., Koonin, E.V., Rudd, K.E., Banuett, F., and Herskowitz, I. 1993. The Escherichia coli hflA locus encodes a putative GTP-binding protein and two membrane proteins, one of which contains a protease-like domain. Proc. Natl. Acad. Sci. U.S.A. 90(22): 10866-10870.
57. Okamoto, S., and Ochi, K. 1998. An essential GTP-binding protein functions as a regulator for differentiation in Streptomyces coelicolor. Mol. Microbiol. 30(1): 107-119.
58. Pillutla, R.C., Sharer, J.D., Gulati, P.S., Wu, E., Yamashita, Y., Lerner, C.G. et al. 1995. Cross-species complementation of the indispensable Escherichia coli era gene highlights amino acid regions essential for activity. J. Bacteriol. 177(8): 2194-2196.
59. Pillutla, R.C., Ahnn, J., and Inouye, M. 1996. Deletion of the putative effector region of Era, an essential GTP-binding protein in Escherichia coli, causes a dominant-negative phenotype. FEMS Microbiol. Lett. 143(1): 47-55.
60. Powell, B.S., Court, D.L., Inada, T., Nakamura, Y., Michotey, V., Cui, X. et al. 1995. Novel proteins of the phosphotransferase system encoded within the rpoN operon of Escherichia coli. Enzyme IIANtr affects growth on organic nitrogen and the conditional lethality of an era ts mutant. J. Biol. Chem. 270(9): 4822-4839.
61. Roberts, R.J. 2004. Identifying protein function - a call for community action. PLoS Biol. 2(3): E42.
62. Roberts, M.W., and Rabinowitz, J.C. 1989. The effect of Escherichia coli ribosomal protein S1 on the translational specificity of bacterial ribosomes. J. Biol. Chem. 264(4): 2228-2235.
63. Robinson, V.L., Hwang, J., Fox, E., Inouye, M., and Stock, A.M. 2002. Domain arrangement of Der, a switch protein containing two GTPase domains. Structure (Cambridge), 10(12): 1649-1658.
64. Saraste, M., Sibbald, P.R., and Wittinghofer, A. 1990. The P-loop - a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15(11): 430-434.
65. Sato, A., Kobayashi, G., Hayashi, H., Yoshida, H., Wada, A., Maeda, M. et al. 2005. The GTP binding protein Obg homolog ObgE is involved in ribosome maturation. Genes Cells, 10(5): 393-408.
66. Sayed, A., Matsuyama, S., and Inouye, M. 1999. Era, an essential Escherichia coli small G-protein, binds to the 30S ribosomal subunit. Biochem. Biophys. Res. Commun. 264(1): 51-54.
67. Scott, J.M., and Haldenwang, W.G. 1999. Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor sigma(B). J. Bacteriol. 181(15): 4653-4660.
68. Scott, J.M., Ju, J., Mitchell, T., and Haldenwang, W.G. 2000. The Bacillus subtilis GTP binding protein obg and regulators of the sigma(B) stress response transcription factor cofractionate with ribosomes. J. Bacteriol. 182(10): 2771-2777.
69. Scrima, A., Vetter, I.R., Armengod, M.E., and Wittinghofer, A. 2005. The structure of the TrmE GTP-binding protein and its implications for tRNA modification. EMBO J. 24(1): 23-33.
70. Sharma, M.R., Barat, C., Wilson, D.N., Booth, T.M., Kawazoe, M., Hori-Takemoto, C. et al. 2005. Interaction of Era with the 30S ribosomal subunit: implications for 30S subunit assembly. Mol. Cell, 18(3): 319-329.
71. Shin, D.H., Lou, Y., Jancarik, J., Yokota, H., Kim, R., and Kim, S.H. 2004. Crystal structure of YjeQ from Thermotoga maritima contains a circularly permuted GTPase domain. Proc. Natl. Acad. Sci. U.S.A. 101(36): 13198-13203.
72. Slominska, M., Konopa, G., Wegrzyn, G., and Czyz, A. 2002. Impaired chromosome partitioning and synchronization of DNA replication initiation in an insertional mutant in the Vibrio harveyi cgtA gene coding for a common GTP-binding protein. Biochem. J. 362(Pt 3): 579-584.
73. Sullivan, S.M., Mishra, R., Neubig, R.R., and Maddock, J.R. 2000. Analysis of guanine nucleotide binding and exchange kinetics of the Escherichia coli GTPase Era. J. Bacteriol. 182(12): 3460-3466.
74. Tan, J., Jakob, U., and Bardwell, J.C. 2002. Overexpression of two different GTPases rescues a null mutation in a heat-induced rRNA methyltransferase. J. Bacteriol. 184(10): 2692-2698.
75. Tatusov, R.L., Koonin, E.V., and Lipman, D.J. 1997. A genomic perspective on protein families. Science (Washington, D.C.), 278(5338): 631-637.
76. 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(1): 33-36.
77. Tatusov, R.L., Natale, D.A., Garkavtsev, I.V., Tatusova, T.A., Shankavaram, U.T., Rao, B.S. et al. 2001. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29(1): 22-28.
78. Teplyakov, A., Obmolova, G., Chu, S.Y., Toedt, J., Eisenstein, E., Howard, A.J., and Gilliland, G.L. 2003. Crystal structure of the YchF protein reveals binding sites for GTP and nucleic acid. J. Bacteriol. 185(14): 4031-4037.
79. Trach, K., and Hoch, J.A. 1989. The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein. J. Bacteriol. 171(3): 1362-1371.
80. Urbonavicius, J., Stahl, G., Durand, J.M., Ben Salem, S.N., Qian, Q., Farabaugh, P.J., and Bjork, G.R. 2003. Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshifting. RNA, 9(6): 760-768.
81. Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G. et al. 2001. The sequence of the human genome. Science (Washington, D.C.), 291(5507): 1304-1351.
82. Vidwans, S.J., Ireton, K., and Grossman, A.D. 1995. Possible role for the essential GTP-binding protein Obg in regulating the initiation of sporulation in Bacillus subtilis. J. Bacteriol. 177(11): 3308-3311.
83. Walker, J.E., Saraste, M., and Runswick, M.J. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1: 945-951.
84. Wang, B., and Kuramitsu, H.K. 2003. Assessment of the utilization of the antisense RNA strategy to identify essential genes in heterologous bacteria. FEMS Microbiol Lett, 220(2): 171-176.
85. Welsh, K.M., Trach, K.A., Folger, C., and Hoch, J.A. 1994. Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis. J. Bacteriol. 176(23): 7161-7168.
86. Wout, P., Pu, K., Sullivan, S.M., Reese, V., Zhou, S., Lin, B., and Maddock, J.R. 2004. The Escherichia coli GTPase CgtAE cofractionates with the 50S ribosomal subunit and interacts with SpoT, a ppGpp synthetase/hydrolase. J. Bacteriol. 186(16): 5249-5257.
87. Yamanaka, K., Hwang, J., and Inouye, M. 2000. Characterization of GTPase activity of TrmE, a member of a novel GTPase superfamily, from Thermotoga maritima. J. Bacteriol. 182(24): 7078-7082.
88. Yim, L., Martinez-Vicente, M., Villarroya, M., Aguado, C., Knecht, E., and Armengod, M.E. 2003. The GTPase activity and C-terminal cysteine of the Escherichia coli MnmE protein are essential for its tRNA modifying function. J. Biol. Chem. 278(31): 28378-28387.
89. Zhang, S., and Haldenwang, W.G. 2004. Guanine nucleotides stabilize the binding of Bacillus subtilis Obg to ribosomes. Biochem. Biophys. Res. Commun. 322(2): 565-569.
90. Zuber, M., Hoover, T.A., Dertzbaugh, M.T., and Court, D.L. 1997. A Francisella tularensis DNA clone complements Escherichia coli defective for the production of Era, an essential Ras-like GTP-binding protein. Gene, 189(1): 31-34.