Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Jun;173(11):3564–3572. doi: 10.1128/jb.173.11.3564-3572.1991

Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits.

A P Vogler 1, M Homma 1, V M Irikura 1, R M Macnab 1
PMCID: PMC207973  PMID: 1646201

Abstract

Many flagellar proteins are exported by a flagellum-specific export pathway. In an initial attempt to characterize the apparatus responsible for the process, we designed a simple assay to screen for mutants with export defects. Temperature-sensitive flagellar mutants of Salmonella typhimurium were grown at the permissive temperature (30 degrees C), shifted to the restrictive temperature (42 degrees C), and inspected in a light microscope. With the exception of switch mutants, they were fully motile. Next, cells grown at the permissive temperature had their flagellar filaments removed by shearing before the cells were shifted to the restrictive temperature. Most mutants were able to regrow filaments. However, flhA, fliH, fliI, and fliN mutants showed no or greatly reduced regrowth, suggesting that the corresponding gene products are involved in the process of flagellum-specific export. We describe here the sequences of fliH, fliI, and the adjacent gene, fliJ; they encode proteins with deduced molecular masses of 25,782, 49,208, and 17,302 Da, respectively. The deduced sequence of FliI shows significant similarity to the catalytic beta subunit of the bacterial F0F1 ATPase and to the catalytic subunits of vacuolar and archaebacterial ATPases; except for limited similarity in the motifs that constitute the nucleotide-binding or catalytic site, it appears unrelated to the E1E2 class of ATPases, to other proteins that mediate protein export, or to a variety of other ATP-utilizing enzymes. We hypothesize that FliI is either the catalytic subunit of a protein translocase for flagellum-specific export or a proton translocase involved in local circuits at the flagellum.

Full text

PDF
3564

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aizawa S. I., Dean G. E., Jones C. J., Macnab R. M., Yamaguchi S. Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium. J Bacteriol. 1985 Mar;161(3):836–849. doi: 10.1128/jb.161.3.836-849.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albertini A. M., Caramori T., Crabb W. D., Scoffone F., Galizzi A. The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide. J Bacteriol. 1991 Jun;173(11):3573–3579. doi: 10.1128/jb.173.11.3573-3579.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aswad D., Koshland D. E., Jr Isolation, characterization and complementation of Salmonella typhimurium chemotaxis mutants. J Mol Biol. 1975 Sep 15;97(2):225–235. doi: 10.1016/s0022-2836(75)80036-2. [DOI] [PubMed] [Google Scholar]
  4. Bartlett D. H., Frantz B. B., Matsumura P. Flagellar transcriptional activators FlbB and FlaI: gene sequences and 5' consensus sequences of operons under FlbB and FlaI control. J Bacteriol. 1988 Apr;170(4):1575–1581. doi: 10.1128/jb.170.4.1575-1581.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowman B. J., Allen R., Wechser M. A., Bowman E. J. Isolation of genes encoding the Neurospora vacuolar ATPase. Analysis of vma-2 encoding the 57-kDa polypeptide and comparison to vma-1. J Biol Chem. 1988 Oct 5;263(28):14002–14007. [PubMed] [Google Scholar]
  6. Bowman E. J., Tenney K., Bowman B. J. Isolation of genes encoding the Neurospora vacuolar ATPase. Analysis of vma-1 encoding the 67-kDa subunit reveals homology to other ATPases. J Biol Chem. 1988 Oct 5;263(28):13994–14001. [PubMed] [Google Scholar]
  7. Cerretti D. P., Dean D., Davis G. R., Bedwell D. M., Nomura M. The spc ribosomal protein operon of Escherichia coli: sequence and cotranscription of the ribosomal protein genes and a protein export gene. Nucleic Acids Res. 1983 May 11;11(9):2599–2616. doi: 10.1093/nar/11.9.2599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chen C. J., Chin J. E., Ueda K., Clark D. P., Pastan I., Gottesman M. M., Roninson I. B. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell. 1986 Nov 7;47(3):381–389. doi: 10.1016/0092-8674(86)90595-7. [DOI] [PubMed] [Google Scholar]
  9. Chou P. Y., Fasman G. D. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. doi: 10.1002/9780470122921.ch2. [DOI] [PubMed] [Google Scholar]
  10. Cossart P., Katinka M., Yaniv M. Nucleotide sequence of the thrB gene of E. coli, and its two adjacent regions; the thrAB and thrBC junctions. Nucleic Acids Res. 1981 Jan 24;9(2):339–347. doi: 10.1093/nar/9.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
  12. Dean G. E., Aizawa S. I., Macnab R. M. flaAII (motC, cheV) of Salmonella typhimurium is a structural gene involved in energization and switching of the flagellar motor. J Bacteriol. 1983 Apr;154(1):84–91. doi: 10.1128/jb.154.1.84-91.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dean G. E., Macnab R. M., Stader J., Matsumura P., Burks C. Gene sequence and predicted amino acid sequence of the motA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli. J Bacteriol. 1984 Sep;159(3):991–999. doi: 10.1128/jb.159.3.991-999.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Denda K., Konishi J., Oshima T., Date T., Yoshida M. Molecular cloning of the beta-subunit of a possible non-F0F1 type ATP synthase from the acidothermophilic archaebacterium, Sulfolobus acidocaldarius. J Biol Chem. 1988 Nov 25;263(33):17251–17254. [PubMed] [Google Scholar]
  15. Denda K., Konishi J., Oshima T., Date T., Yoshida M. The membrane-associated ATPase from Sulfolobus acidocaldarius is distantly related to F1-ATPase as assessed from the primary structure of its alpha-subunit. J Biol Chem. 1988 May 5;263(13):6012–6015. [PubMed] [Google Scholar]
  16. Downing W. L., Sullivan S. L., Gottesman M. E., Dennis P. P. Sequence and transcriptional pattern of the essential Escherichia coli secE-nusG operon. J Bacteriol. 1990 Mar;172(3):1621–1627. doi: 10.1128/jb.172.3.1621-1627.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dunn S. D., Heppel L. A. Properties and functions of the subunits of the Escherichia coli coupling factor ATPase. Arch Biochem Biophys. 1981 Sep;210(2):421–436. doi: 10.1016/0003-9861(81)90206-x. [DOI] [PubMed] [Google Scholar]
  18. Eisenbach M. Functions of the flagellar modes of rotation in bacterial motility and chemotaxis. Mol Microbiol. 1990 Feb;4(2):161–167. doi: 10.1111/j.1365-2958.1990.tb00584.x. [DOI] [PubMed] [Google Scholar]
  19. Emerson S. U., Tokuyasu K., Simon M. I. Bacterial flagella: polarity of elongation. Science. 1970 Jul 10;169(3941):190–192. doi: 10.1126/science.169.3941.190. [DOI] [PubMed] [Google Scholar]
  20. Engelman D. M., Steitz T. A., Goldman A. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem. 1986;15:321–353. doi: 10.1146/annurev.bb.15.060186.001541. [DOI] [PubMed] [Google Scholar]
  21. Felmlee T., Pellett S., Welch R. A. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol. 1985 Jul;163(1):94–105. doi: 10.1128/jb.163.1.94-105.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fickett J. W. Recognition of protein coding regions in DNA sequences. Nucleic Acids Res. 1982 Sep 11;10(17):5303–5318. doi: 10.1093/nar/10.17.5303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fujita H., Yamaguchi S., Taira T., Iino T. A simple method for the isolation of flagellar shape mutants in Salmonella. J Gen Microbiol. 1981 Jul;125(1):213–216. doi: 10.1099/00221287-125-1-213. [DOI] [PubMed] [Google Scholar]
  24. Futai M., Noumi T., Maeda M. ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu Rev Biochem. 1989;58:111–136. doi: 10.1146/annurev.bi.58.070189.000551. [DOI] [PubMed] [Google Scholar]
  25. Garrido M. C., Herrero M., Kolter R., Moreno F. The export of the DNA replication inhibitor Microcin B17 provides immunity for the host cell. EMBO J. 1988 Jun;7(6):1853–1862. doi: 10.1002/j.1460-2075.1988.tb03018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gay N. J., Walker J. E. The atp operon: nucleotide sequence of the region encoding the alpha-subunit of Escherichia coli ATP-synthase. Nucleic Acids Res. 1981 May 11;9(9):2187–2194. doi: 10.1093/nar/9.9.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hess J. F., Oosawa K., Kaplan N., Simon M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell. 1988 Apr 8;53(1):79–87. doi: 10.1016/0092-8674(88)90489-8. [DOI] [PubMed] [Google Scholar]
  28. Hesse J. E., Wieczorek L., Altendorf K., Reicin A. S., Dorus E., Epstein W. Sequence homology between two membrane transport ATPases, the Kdp-ATPase of Escherichia coli and the Ca2+-ATPase of sarcoplasmic reticulum. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4746–4750. doi: 10.1073/pnas.81.15.4746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Higgins C. F., Haag P. D., Nikaido K., Ardeshir F., Garcia G., Ames G. F. Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature. 1982 Aug 19;298(5876):723–727. doi: 10.1038/298723a0. [DOI] [PubMed] [Google Scholar]
  30. Homma M., DeRosier D. J., Macnab R. M. Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J Mol Biol. 1990 Jun 20;213(4):819–832. doi: 10.1016/S0022-2836(05)80266-9. [DOI] [PubMed] [Google Scholar]
  31. Homma M., Fujita H., Yamaguchi S., Iino T. Excretion of unassembled flagellin by Salmonella typhimurium mutants deficient in hook-associated proteins. J Bacteriol. 1984 Sep;159(3):1056–1059. doi: 10.1128/jb.159.3.1056-1059.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Homma M., Iino T., Macnab R. M. Identification and characterization of the products of six region III flagellar genes (flaAII.3 through flaQII) of Salmonella typhimurium. J Bacteriol. 1988 May;170(5):2221–2228. doi: 10.1128/jb.170.5.2221-2228.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Homma M., Komeda Y., Iino T., Macnab R. M. The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J Bacteriol. 1987 Apr;169(4):1493–1498. doi: 10.1128/jb.169.4.1493-1498.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Homma M., Kutsukake K., Hasebe M., Iino T., Macnab R. M. FlgB, FlgC, FlgF and FlgG. A family of structurally related proteins in the flagellar basal body of Salmonella typhimurium. J Mol Biol. 1990 Jan 20;211(2):465–477. doi: 10.1016/0022-2836(90)90365-S. [DOI] [PubMed] [Google Scholar]
  35. Homma M., Kutsukake K., Iino T., Yamaguchi S. Hook-associated proteins essential for flagellar filament formation in Salmonella typhimurium. J Bacteriol. 1984 Jan;157(1):100–108. doi: 10.1128/jb.157.1.100-108.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Homma M., Ohnishi K., Iino T., Macnab R. M. Identification of flagellar hook and basal body gene products (FlaFV, FlaFVI, FlaFVII and FlaFVIII) in Salmonella typhimurium. J Bacteriol. 1987 Aug;169(8):3617–3624. doi: 10.1128/jb.169.8.3617-3624.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Iino T. Assembly of Salmonella flagellin in vitro and in vivo. J Supramol Struct. 1974;2(2-4):372–384. doi: 10.1002/jss.400020226. [DOI] [PubMed] [Google Scholar]
  38. Iino T., Komeda Y., Kutsukake K., Macnab R. M., Matsumura P., Parkinson J. S., Simon M. I., Yamaguchi S. New unified nomenclature for the flagellar genes of Escherichia coli and Salmonella typhimurium. Microbiol Rev. 1988 Dec;52(4):533–535. doi: 10.1128/mr.52.4.533-535.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Iino T. Polarity of flagellar growth in salmonella. J Gen Microbiol. 1969 May;56(2):227–239. doi: 10.1099/00221287-56-2-227. [DOI] [PubMed] [Google Scholar]
  40. Ikeda T., Asakura S., Kamiya R. Total reconstitution of Salmonella flagellar filaments from hook and purified flagellin and hook-associated proteins in vitro. J Mol Biol. 1989 Sep 5;209(1):109–114. doi: 10.1016/0022-2836(89)90174-5. [DOI] [PubMed] [Google Scholar]
  41. Inatomi K., Eya S., Maeda M., Futai M. Amino acid sequence of the alpha and beta subunits of Methanosarcina barkeri ATPase deduced from cloned genes. Similarity to subunits of eukaryotic vacuolar and F0F1-ATPases. J Biol Chem. 1989 Jul 5;264(19):10954–10959. [PubMed] [Google Scholar]
  42. Jones C. J., Homma M., Macnab R. M. L-, P-, and M-ring proteins of the flagellar basal body of Salmonella typhimurium: gene sequences and deduced protein sequences. J Bacteriol. 1989 Jul;171(7):3890–3900. doi: 10.1128/jb.171.7.3890-3900.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Jones C. J., Macnab R. M. Flagellar assembly in Salmonella typhimurium: analysis with temperature-sensitive mutants. J Bacteriol. 1990 Mar;172(3):1327–1339. doi: 10.1128/jb.172.3.1327-1339.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Jones C. J., Macnab R. M., Okino H., Aizawa S. Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J Mol Biol. 1990 Mar 20;212(2):377–387. doi: 10.1016/0022-2836(90)90132-6. [DOI] [PubMed] [Google Scholar]
  45. Joys T. M. The covalent structure of the phase-1 flagellar filament protein of Salmonella typhimurium and its comparison with other flagellins. J Biol Chem. 1985 Dec 15;260(29):15758–15761. [PubMed] [Google Scholar]
  46. Kanazawa H., Kayano T., Mabuchi K., Futai M. Nucleotide sequence of the genes coding for alpha, beta and gamma subunits of the proton-translocating ATPase of Escherichia coli. Biochem Biophys Res Commun. 1981 Nov 30;103(2):604–612. doi: 10.1016/0006-291x(81)90494-0. [DOI] [PubMed] [Google Scholar]
  47. Kihara M., Homma M., Kutsukake K., Macnab R. M. Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences. J Bacteriol. 1989 Jun;171(6):3247–3257. doi: 10.1128/jb.171.6.3247-3257.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Krikos A., Mutoh N., Boyd A., Simon M. I. Sensory transducers of E. coli are composed of discrete structural and functional domains. Cell. 1983 Jun;33(2):615–622. doi: 10.1016/0092-8674(83)90442-7. [DOI] [PubMed] [Google Scholar]
  49. Kuby S. A., Palmieri R. H., Frischat A., Fischer A. H., Wu L. H., Maland L., Manship M. Studies on adenosine triphosphate transphosphorylases. Amino acid sequence of rabbit muscle ATP-AMP transphosphorylase. Biochemistry. 1984 May 22;23(11):2393–2399. doi: 10.1021/bi00306a012. [DOI] [PubMed] [Google Scholar]
  50. Kuchler K., Sterne R. E., Thorner J. Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells. EMBO J. 1989 Dec 20;8(13):3973–3984. doi: 10.1002/j.1460-2075.1989.tb08580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Kumamoto C. A., Nault A. K. Characterization of the Escherichia coli protein-export gene secB. Gene. 1989 Jan 30;75(1):167–175. doi: 10.1016/0378-1119(89)90393-4. [DOI] [PubMed] [Google Scholar]
  52. Kuo S. C., Koshland D. E., Jr Sequence of the flaA (cheC) locus of Escherichia coli and discovery of a new gene. J Bacteriol. 1986 Jun;166(3):1007–1012. doi: 10.1128/jb.166.3.1007-1012.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Kutsukake K., Ohya Y., Yamaguchi S., Iino T. Operon structure of flagellar genes in Salmonella typhimurium. Mol Gen Genet. 1988 Sep;214(1):11–15. doi: 10.1007/BF00340172. [DOI] [PubMed] [Google Scholar]
  54. Kuwajima G., Asaka J., Fujiwara T., Fujiwara T., Node K., Kondo E. Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. J Bacteriol. 1986 Dec;168(3):1479–1483. doi: 10.1128/jb.168.3.1479-1483.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Kuwajima G., Kawagishi I., Homma M., Asaka J., Kondo E., Macnab R. M. Export of an N-terminal fragment of Escherichia coli flagellin by a flagellum-specific pathway. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4953–4957. doi: 10.1073/pnas.86.13.4953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  57. Macnab R. M. Examination of bacterial flagellation by dark-field microscopy. J Clin Microbiol. 1976 Sep;4(3):258–265. doi: 10.1128/jcm.4.3.258-265.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Macnab R. M. The end of the line in bacterial sensing: the flagellar motor. Cold Spring Harb Symp Quant Biol. 1988;53(Pt 1):67–75. doi: 10.1101/sqb.1988.053.01.011. [DOI] [PubMed] [Google Scholar]
  59. Malakooti J., Komeda Y., Matsumura P. DNA sequence analysis, gene product identification, and localization of flagellar motor components of Escherichia coli. J Bacteriol. 1989 May;171(5):2728–2734. doi: 10.1128/jb.171.5.2728-2734.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. McGrath J. P., Varshavsky A. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature. 1989 Aug 3;340(6232):400–404. doi: 10.1038/340400a0. [DOI] [PubMed] [Google Scholar]
  61. Mutoh N., Simon M. I. Nucleotide sequence corresponding to five chemotaxis genes in Escherichia coli. J Bacteriol. 1986 Jan;165(1):161–166. doi: 10.1128/jb.165.1.161-166.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Namba K., Yamashita I., Vonderviszt F. Structure of the core and central channel of bacterial flagella. Nature. 1989 Dec 7;342(6250):648–654. doi: 10.1038/342648a0. [DOI] [PubMed] [Google Scholar]
  63. Ohnishi K., Kutsukake K., Suzuki H., Iino T. Gene fliA encodes an alternative sigma factor specific for flagellar operons in Salmonella typhimurium. Mol Gen Genet. 1990 Apr;221(2):139–147. doi: 10.1007/BF00261713. [DOI] [PubMed] [Google Scholar]
  64. Patterson-Delafield J., Martinez R. J., Stocker B. A., Yamaguchi S. A new fla gene in Salmonella typhimurium--flaR--and its mutant phenotype-superhooks. Arch Mikrobiol. 1973 Mar 26;90(2):107–120. doi: 10.1007/BF00414513. [DOI] [PubMed] [Google Scholar]
  65. Russo A. F., Koshland D. E., Jr Separation of signal transduction and adaptation functions of the aspartate receptor in bacterial sensing. Science. 1983 Jun 3;220(4601):1016–1020. doi: 10.1126/science.6302843. [DOI] [PubMed] [Google Scholar]
  66. Sancar A., Stachelek C., Konigsberg W., Rupp W. D. Sequences of the recA gene and protein. Proc Natl Acad Sci U S A. 1980 May;77(5):2611–2615. doi: 10.1073/pnas.77.5.2611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Saraste M., Gay N. J., Eberle A., Runswick M. J., Walker J. E. The atp operon: nucleotide sequence of the genes for the gamma, beta, and epsilon subunits of Escherichia coli ATP synthase. Nucleic Acids Res. 1981 Oct 24;9(20):5287–5296. doi: 10.1093/nar/9.20.5287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Schmidt M. G., Rollo E. E., Grodberg J., Oliver D. B. Nucleotide sequence of the secA gene and secA(Ts) mutations preventing protein export in Escherichia coli. J Bacteriol. 1988 Aug;170(8):3404–3414. doi: 10.1128/jb.170.8.3404-3414.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Senior A. E. The proton-translocating ATPase of Escherichia coli. Annu Rev Biophys Biophys Chem. 1990;19:7–41. doi: 10.1146/annurev.bb.19.060190.000255. [DOI] [PubMed] [Google Scholar]
  71. Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Shoji S., Ericsson L. H., Walsh K. A., Fischer E. H., Titani K. Amino acid sequence of the catalytic subunit of bovine type II adenosine cyclic 3',5'-phosphate dependent protein kinase. Biochemistry. 1983 Jul 19;22(15):3702–3709. doi: 10.1021/bi00284a025. [DOI] [PubMed] [Google Scholar]
  73. Silverman M. R., Simon M. I. Flagellar assembly mutants in Escherichia coli. J Bacteriol. 1972 Nov;112(2):986–993. doi: 10.1128/jb.112.2.986-993.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Stader J., Matsumura P., Vacante D., Dean G. E., Macnab R. M. Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane. J Bacteriol. 1986 Apr;166(1):244–252. doi: 10.1128/jb.166.1.244-252.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Stock A., Chen T., Welsh D., Stock J. CheA protein, a central regulator of bacterial chemotaxis, belongs to a family of proteins that control gene expression in response to changing environmental conditions. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1403–1407. doi: 10.1073/pnas.85.5.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Stock A., Koshland D. E., Jr, Stock J. Homologies between the Salmonella typhimurium CheY protein and proteins involved in the regulation of chemotaxis, membrane protein synthesis, and sporulation. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7989–7993. doi: 10.1073/pnas.82.23.7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Suzuki T., Iino T., Horiguchi T., Yamaguchi S. Incomplete flagellar structures in nonflagellate mutants of Salmonella typhimurium. J Bacteriol. 1978 Feb;133(2):904–915. doi: 10.1128/jb.133.2.904-915.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Suzuki T., Komeda Y. Incomplete flagellar structures in Escherichia coli mutants. J Bacteriol. 1981 Feb;145(2):1036–1041. doi: 10.1128/jb.145.2.1036-1041.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Walker J. E., Saraste M., Runswick M. J., Gay N. J. 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. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Yamaguchi S., Aizawa S., Kihara M., Isomura M., Jones C. J., Macnab R. M. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol. 1986 Dec;168(3):1172–1179. doi: 10.1128/jb.168.3.1172-1179.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Yamaguchi S., Fujita H., Ishihara A., Aizawa S., Macnab R. M. Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching. J Bacteriol. 1986 Apr;166(1):187–193. doi: 10.1128/jb.166.1.187-193.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES