Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti
10.1128/jb.179.20.6391-6399.1997
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

The peritrichous flagella of Rhizobium meliloti rotate only clockwise and control directional changes of swimming cells by modulating flagellar rotary speed. Using Tn5 insertions, we have identified and sequenced a motility (mot) operon containing three genes, motB, motC, and motD, that are translationally coupled. The motB gene (and an unlinked motA) has been assigned by similarity to the Escherichia coli and Bacillus subtilis homologs, whereas motC and motD are new and without known precedents in other bacteria. In-frame deletions introduced in motB, motC, or motD each result in paralysis. MotD function was fully restored by complementation with the wild-type motD gene. By contrast, deletions in motB or motC required the native combination of motB and motC in trans for restoring normal flagellar rotation, whereas complementation with motB or motC alone led to uncoordinated (jiggly) swimming. Similarly, a motB-motC gene fusion and a Tn5 insertion intervening between motB and motC resulted in jiggly swimming as a consequence of large fluctuations in flagellar rotary speed. We conclude that MotC biosynthesis requires coordinate expression of motB and motC and balanced amounts of the two gene products. The MotC polypeptide contains an N-terminal signal sequence for export, and Western blots have confirmed its location in the periplasm of the R. meliloti cell. A working model suggests that interactions between MotB and MotC at the periplasmic surface of the motor control the energy flux or the energy coupling that drives flagellar rotation.

Bibliography

Platzer, J., Sterr, W., Hausmann, M., & Schmitt, R. (1997). Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti. Journal of Bacteriology, 179(20), 6391–6399.

Authors 4
  1. J Platzer (first)
  2. W Sterr (additional)
  3. M Hausmann (additional)
  4. R Schmitt (additional)
References 68 Referenced 69
  1. Bachmann , B. J. 1990 . Linkage map of Escherichia coli K-12, edition 8 . Microbiol. Rev. 54 : 130 - 197 . (10.1128/mr.54.2.130-197.1990) / Microbiol. Rev. / Linkage map of Escherichia coli K-12, edition 8 by Bachmann B. J. (1990)
  2. Blair , D. F. , and H. C. Berg . 1988 . Restoration of torque in defective flagellar motors . Science 242 : 1678 - 1681 . (10.1126/science.2849208) / Science / Restoration of torque in defective flagellar motors by Blair D. F. (1988)
  3. Blair , D. F. , and H. C. Berg . 1990 . The MotA protein of E. coli is a protonconducting component of the flagellar motor . Cell 60 : 439 - 449 . (10.1016/0092-8674(90)90595-6) / Cell / The MotA protein of E. coli is a protonconducting component of the flagellar motor by Blair D. F. (1990)
  4. Blair , D. F. , and H. C. Berg . 1991 . Mutations in the MotA protein of Escherichia coli reveal domains critical for proton conduction . J. Mol. Biol. 221 : 1433 - 1442 . (10.1016/0022-2836(91)90943-Z) / J. Mol. Biol. / Mutations in the MotA protein of Escherichia coli reveal domains critical for proton conduction by Blair D. F. (1991)
  5. Blair , D. F. , D. Y. Kim , and H. C. Berg . 1991 . Mutant MotB proteins in Escherichia coli . J. Bacteriol. 173 : 4049 - 4055 . (10.1128/jb.173.13.4049-4055.1991) / J. Bacteriol. / Mutant MotB proteins in Escherichia coli by Blair D. F. (1991)
  6. Brickman , E. , and J. Beckwith . 1975 . Analysis of the regulation of E. coli alkaline phosphatase synthesis using deletions and 80 transducing phages . J. Mol. Biol. 96 : 307 - 316 . (10.1016/0022-2836(75)90350-2) / J. Mol. Biol. / Analysis of the regulation of E. coli alkaline phosphatase synthesis using deletions and 80 transducing phages by Brickman E. (1975)
  7. Chun , S. Y. , and J. S. Parkinson . 1988 . Bacterial motility: membrane topology of the Escherichia coli MotB protein . Science 239 : 276 - 278 . (10.1126/science.2447650) / Science / Bacterial motility: membrane topology of the Escherichia coli MotB protein by Chun S. Y. (1988)
  8. Dean , G. E. , R. M. Macnab , J. Stader , P. Matsumura , and C. Burks . 1984 . Gene sequence and predicted amino acid sequence of the motA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli . J. Bacteriol. 159 : 991 - 999 . (10.1128/jb.159.3.991-999.1984) / J. Bacteriol. / Gene sequence and predicted amino acid sequence of the motA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli by Dean G. E. (1984)
  9. De Mot , R. , and J. Vanderleyden . 1994 . The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan . Mol. Microbiol. 12 : 333 - 334 . (10.1111/j.1365-2958.1994.tb01021.x) / Mol. Microbiol. / The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan by De Mot R. (1994)
  10. Devereux , J. , P. Haeberli , and O. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 . (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX by Devereux J. (1984)
  11. Dietmaier , W. , S. Fabry , and R. Schmitt . 1993 . DISEC-TRISEC: di- and trinucleotide-sticky-end cloning of PCR-amplified DNA . Nucleic Acids Res. 21 : 3603 - 3604 . (10.1093/nar/21.15.3603) / Nucleic Acids Res. / DISEC-TRISEC: di- and trinucleotide-sticky-end cloning of PCR-amplified DNA by Dietmaier W. (1993)
  12. Fields , S. , and O. Song . 1989 . A novel genetic system to detect proteinprotein interactions . Nature 340 : 240 - 241 . (10.1038/340245a0) / Nature / A novel genetic system to detect proteinprotein interactions by Fields S. (1989)
  13. Francis , N. R. , G. E. Sosinsky , D. Thomas , and D. J. DeRosier . 1994 . Isolation, characterisation and structure of bacterial flagellar motors containing the switch complex . J. Mol. Biol. 235 : 1261 - 1270 . (10.1006/jmbi.1994.1079) / J. Mol. Biol. / Isolation, characterisation and structure of bacterial flagellar motors containing the switch complex by Francis N. R. (1994)
  14. Götz , R. , N. Limmer , K. Ober , and R. Schmitt . 1982 . Motility and chemotaxis in two strains of Rhizobium with complex flagella . J. Gen. Microbiol. 128 : 789 - 798 . / J. Gen. Microbiol. / Motility and chemotaxis in two strains of Rhizobium with complex flagella by Götz R. (1982)
  15. Götz , R. , and R. Schmitt . 1987 . Rhizobium meliloti swims by unidirectional, intermittent rotation of right-handed flagellar helices . J. Bacteriol. 169 : 3146 - 3150 . (10.1128/jb.169.7.3146-3150.1987) / J. Bacteriol. / Rhizobium meliloti swims by unidirectional, intermittent rotation of right-handed flagellar helices by Götz R. (1987)
  16. Greck , M. , J. Platzer , V. Sourjik , and R. Schmitt . 1995 . Analysis of a chemotaxis operon in Rhizobium meliloti . Mol. Microbiol. 15 : 989 - 1000 . (10.1111/j.1365-2958.1995.tb02274.x) / Mol. Microbiol. / Analysis of a chemotaxis operon in Rhizobium meliloti by Greck M. (1995)
  17. Haslbeck M. W. Sterr and R. Schmitt. Unpublished data.
  18. Helmann , J. D. 1991 . Alternative sigma factors and the regulation of flagellar gene expression . Mol. Microbiol. 5 : 2875 - 2882 . (10.1111/j.1365-2958.1991.tb01847.x) / Mol. Microbiol. / Alternative sigma factors and the regulation of flagellar gene expression by Helmann J. D. (1991)
  19. Higuchi R. 1989. Using PCR to engineer DNA p. 61-70. In H. A. Erlich (ed.) PCR technology. Principles and applications for DNA amplification. Stockton Press New York N.Y. (10.1007/978-1-349-20235-5_6)
  20. Hirota , N. , and Y. Imae . 1983 . Na~-driven flagellar motors of an alkalophilic Bacillus strain YN-1 . J. Mol. Biol. Chem. 258 : 10557 - 10581 . / J. Mol. Biol. Chem. / Na~-driven flagellar motors of an alkalophilic Bacillus strain YN-1 by Hirota N. (1983)
  21. Irikura , V. M. , M. Kihara , S. Yamaguchi , H. Sockett , and R. M. Macnab . 1993 . Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor . J. Bacteriol. 175 : 802 - 810 . (10.1128/jb.175.3.802-810.1993) / J. Bacteriol. / Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor by Irikura V. M. (1993)
  22. Jones , C. J. , and S. Aizawa . 1991 . The bacterial flagellum and flagellar motor: structure, assembly and function . Adv. Microb. Physiol. 32 : 109 - 172 . (10.1016/S0065-2911(08)60007-7) / Adv. Microb. Physiol. / The bacterial flagellum and flagellar motor: structure, assembly and function by Jones C. J. (1991)
  23. Kamberger , W. 1979 . An Ouchterlony double diffusion study on the interaction between legume lectins and rhizobial cell surface antigens . Arch. Microbiol. 121 : 83 - 90 . (10.1007/BF00409209) / Arch. Microbiol. / An Ouchterlony double diffusion study on the interaction between legume lectins and rhizobial cell surface antigens by Kamberger W. (1979)
  24. Khan , S. , M. Dapice , and T. H. Reese . 1988 . Effects of mot gene expression on the structure of the flagellar motor . J. Mol. Biol. 202 : 575 - 584 . (10.1016/0022-2836(88)90287-2) / J. Mol. Biol. / Effects of mot gene expression on the structure of the flagellar motor by Khan S. (1988)
  25. Kihara , M. , M. Homma , K. Kutsukake , and R. M. Macnab . 1989 . Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences . J. Bacteriol. 171 : 3247 - 3257 . (10.1128/jb.171.6.3247-3257.1989) / J. Bacteriol. / Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences by Kihara M. (1989)
  26. Koebnik , R. 1995 . Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins . Mol. Microbiol. 16 : 1269 - 1270 . (10.1111/j.1365-2958.1995.tb02348.x) / Mol. Microbiol. / Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins by Koebnik R. (1995)
  27. Krupski , G. , R. Götz , K. Ober , E. Pleier , and R. Schmitt . 1985 . Structure of complex flagellar filaments in Rhizobium meliloti . J. Bacteriol. 162 : 361 - 366 . (10.1128/jb.162.1.361-366.1985) / J. Bacteriol. / Structure of complex flagellar filaments in Rhizobium meliloti by Krupski G. (1985)
  28. Kyte , J. , and R. F. Doolittle . 1982 . A simple method for displaying the hydropathic character of a protein . J. Mol. Biol. 157 : 105 - 132 . (10.1016/0022-2836(82)90515-0) / J. Mol. Biol. / A simple method for displaying the hydropathic character of a protein by Kyte J. (1982)
  29. Labes , M. , A. Pühler , and R. Simon . 1990 . A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria . Gene 89 : 37 - 46 . (10.1016/0378-1119(90)90203-4) / Gene / A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria by Labes M. (1990)
  30. Larsen , S. H. , R. W. Reader , E. N. Kort , W. -W. Tso , and J. Adler . 1974 . Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli . Nature 249 : 74 - 77 . (10.1038/249074a0) / Nature / Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli by Larsen S. H. (1974)
  31. Lehrer , R. J. , A. Barton , and T. Ganz . 1988 . Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple-wave length spectrophotometry . J. Immunol. Methods 108 : 153 - 158 . (10.1016/0022-1759(88)90414-0) / J. Immunol. Methods / Concurrent assessment of inner and outer membrane permeabilization and bacteriolysis in E. coli by multiple-wave length spectrophotometry by Lehrer R. J. (1988)
  32. Li , M. , and H. P. Schweizer . 1993 . Resolution of common DNA sequencing ambiguities of GC-rich DNA templates by terminal deoxynucleotidyl transferase without dGTP analogues . Focus 14/15 : 19 - 20 . / Focus / Resolution of common DNA sequencing ambiguities of GC-rich DNA templates by terminal deoxynucleotidyl transferase without dGTP analogues by Li M. (1993)
  33. Long , S. , S. McCune , and G. C. Walker . 1988 . Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis . J. Bacteriol. 170 : 4257 - 4265 . (10.1128/jb.170.9.4257-4265.1988) / J. Bacteriol. / Symbiotic loci of Rhizobium meliloti identified by random TnphoA mutagenesis by Long S. (1988)
  34. Luria , S. E. , F. N. Adams , and R. C. Ting . 1960 . Transduction of lactose utilizing ability among strains of E. coli and S. dysenteriae and the properties of the transducing phage particles . Virology 12 : 348 - 390 . (10.1016/0042-6822(60)90161-6) / Virology / Transduction of lactose utilizing ability among strains of E. coli and S. dysenteriae and the properties of the transducing phage particles by Luria S. E. (1960)
  35. Macnab R. M. 1996. Flagella and motility p. 123-145. In F. C. Neidhardt R. Curtiss III J. L. Ingraham E. C. C. Lin K. B. Low B. Magasanik W. S. Reznikoff M. Riley M. Schaechter and H. E. Umbarger (ed.) Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. American Society for Microbiology Washington D.C.
  36. Malakooti , J. , Y. Komeda , and P. Matsumara . 1989 . DNA sequence analysis, gene product identification, and localization of flagellar motor components of Escherichia coli . J. Bacteriol. 171 : 2728 - 2734 . (10.1128/jb.171.5.2728-2734.1989) / J. Bacteriol. / DNA sequence analysis, gene product identification, and localization of flagellar motor components of Escherichia coli by Malakooti J. (1989)
  37. Manson , M. D. , P. Tedesco , H. C. Berg , F. M. Harold , and C. van der Driftc . 1977 . A proton motive force drives bacterial flagella . Proc. Natl. Acad. Sci. USA 74 : 3060 - 3064 . (10.1073/pnas.74.7.3060) / Proc. Natl. Acad. Sci. USA / A proton motive force drives bacterial flagella by Manson M. D. (1977)
  38. Marsh , J. L. , M. Erfle , and E. J. Wykes . 1984 . The plC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation . Gene 32 : 482 - 485 . (10.1016/0378-1119(84)90022-2) / Gene / The plC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation by Marsh J. L. (1984)
  39. Martin , J. L. , G. Waksman , J. C. A. Bardwell , J. Beckwith , and J. Kuriyan . 1993 . Crystallization of DsbA, an E. coli protein required for disulphide band formation in vivo . J. Mol. Biol. 230 : 1097 - 1100 . (10.1006/jmbi.1993.1226) / J. Mol. Biol. / Crystallization of DsbA, an E. coli protein required for disulphide band formation in vivo by Martin J. L. (1993)
  40. Maruyama , M. , G. Lodderstaedt , and R. Schmitt . 1978 . Purification and biochemical properties of complex flagella isolated from Rhizobium Iupini H13-3 . Biochim. Biophys. Acta 535 : 110 - 124 . (10.1016/0005-2795(78)90038-7) / Biochim. Biophys. Acta / Purification and biochemical properties of complex flagella isolated from Rhizobium Iupini H13-3 by Maruyama M. (1978)
  41. Matsuura , S. , J. Shioi , and Y. Imae . 1977 . Motility in Bacillus subtilis driven by an artificial proton motive force . FEBS Lett. 82 : 187 - 190 . (10.1016/0014-5793(77)80581-4) / FEBS Lett. / Motility in Bacillus subtilis driven by an artificial proton motive force by Matsuura S. (1977)
  42. Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
  43. Mirel , D. B. , V. M. Lustre , and M. J. Chamberlin . 1992 . An operon of Bacillus subtilis motility genes transcribed by the sigma-D form of RNA polymerase . J. Bacteriol. 174 : 4197 - 4204 . (10.1128/jb.174.13.4197-4204.1992) / J. Bacteriol. / An operon of Bacillus subtilis motility genes transcribed by the sigma-D form of RNA polymerase by Mirel D. B. (1992)
  44. Novick , R. P. , R. C. Clowes , S. N. Cohen , R. Curtis , N. Datta , and S. Falkow . 1976 . Uniform nomenclature for bacterial plasmids: a proposal . Bacteriol. Rev. 40 : 168 - 189 . (10.1128/br.40.1.168-189.1976) / Bacteriol. Rev. / Uniform nomenclature for bacterial plasmids: a proposal by Novick R. P. (1976)
  45. Olsen , G. J. , C. R. Woese , and R. Overbeek . 1994 . The winds of (evolutionary) change: breathing new life into microbiology . J. Bacteriol. 176 : 1 - 6 . (10.1128/jb.176.1.1-6.1994) / J. Bacteriol. / The winds of (evolutionary) change: breathing new life into microbiology by Olsen G. J. (1994)
  46. Oppenheim , D. S. , and C. Yanofsky . 1980 . Translational coupling during expression of the tryptophan operon of Escherichia coli . Genetics 95 : 785 - 795 . (10.1093/genetics/95.4.785) / Genetics / Translational coupling during expression of the tryptophan operon of Escherichia coli by Oppenheim D. S. (1980)
  47. Pleier , E. , and R. Schmitt . 1989 . Identification and sequence analysis of two related flagellin genes in Rhizobium meliloti . J. Bacteriol. 173 : 1467 - 1476 . (10.1128/jb.171.3.1467-1475.1989) / J. Bacteriol. / Identification and sequence analysis of two related flagellin genes in Rhizobium meliloti by Pleier E. (1989)
  48. Pleier , E. , and R. Schmitt . 1991 . Expression of two Rhizobium meliloti genes and their contribution to the complex filament structure . J. Bacteriol. 173 : 2077 - 2085 . (10.1128/jb.173.6.2077-2085.1991) / J. Bacteriol. / Expression of two Rhizobium meliloti genes and their contribution to the complex filament structure by Pleier E. (1991)
  49. Pugsley , A. P. 1993 . The complete general secretory pathway in gram-negative bacteria . Microbiol. Rev. 57 : 50 - 108 . (10.1128/mr.57.1.50-108.1993) / Microbiol. Rev. / The complete general secretory pathway in gram-negative bacteria by Pugsley A. P. (1993)
  50. Rosenberg , A. H. , B. N. Lade , D. Chui , S. Lin , J. J. Dunn , and F. W. Studier . 1987 . Vectors for selective expression of cloned DNAs by T7 RNA polymerase . Gene 56 : 125 - 135 . (10.1016/0378-1119(87)90165-X) / Gene / Vectors for selective expression of cloned DNAs by T7 RNA polymerase by Rosenberg A. H. (1987)
  51. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
  52. Sanger , F. , S. Nicklen , and A. R. Coulson . 1977 . DNA sequencing with chain-terminating inhibitors . Proc. Natl. Acad. Sci. USA 74 : 5463 - 5467 . (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  53. Schäfer , A. , A. Tauch , W. Jäger , J. Kalinowski , G. Thierbach , and A. Pühler . 1994 . Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum . Gene 145 : 69 - 73 . (10.1016/0378-1119(94)90324-7) / Gene / Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum by Schäfer A. (1994)
  54. Schuster , S. C. , and S. Khan . 1994 . The bacterial flagellar motor. Annu . Rev. Biophys. Biomol. Struct. 23 : 509 - 539 . (10.1146/annurev.bb.23.060194.002453) / Rev. Biophys. Biomol. Struct. / The bacterial flagellar motor. Annu by Schuster S. C. (1994)
  55. Selbitschka , W. , S. Niemann , and A. Pühler . 1993 . Construction of gene replacement vectors for Gram~ bacteria using a genetically modified sacRB gene as positive selection marker . Appl. Microbiol. Biotechnol. 38 : 615 - 618 . (10.1007/BF00182799) / Appl. Microbiol. Biotechnol. / Construction of gene replacement vectors for Gram~ bacteria using a genetically modified sacRB gene as positive selection marker by Selbitschka W. (1993)
  56. Shao Z. J. Platzer and R. Schmitt. Unpublished data.
  57. Shine , J. , and L. Dalgarno . 1974 . The 3~ terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites . Proc. Natl. Acad. Sci. USA 71 : 1342 - 1346 . (10.1073/pnas.71.4.1342) / Proc. Natl. Acad. Sci. USA / The 3~ terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites by Shine J. (1974)
  58. Simon , R. , M. O'Connell , M. Labes , and A. Pühler . 1986 . Plasmid vectors for the genetic analysis and manipulation of rhizobia and other Gram-negative bacteria . Methods Enzymol. 118 : 640 - 659 . (10.1016/0076-6879(86)18106-7) / Methods Enzymol. / Plasmid vectors for the genetic analysis and manipulation of rhizobia and other Gram-negative bacteria by Simon R. (1986)
  59. Sockett , H. , S. Yamaguchi , M. Kihara , V. M. Irikura , and R. M. Macnab . 1992 . Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium . J. Bacteriol. 174 : 793 - 806 . (10.1128/jb.174.3.793-806.1992) / J. Bacteriol. / Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium by Sockett H. (1992)
  60. Sourjik , V. , and R. Schmitt . 1996 . Different roles of CheY1 and CheY2 in the chemotaxis of Rhizobium meliloti . Mol. Microbiol. 22 : 427 - 436 . (10.1046/j.1365-2958.1996.1291489.x) / Mol. Microbiol. / Different roles of CheY1 and CheY2 in the chemotaxis of Rhizobium meliloti by Sourjik V. (1996)
  61. Stader , J. , P. Matsumura , D. Vacante , G. E. Dean , and R. M. Macnab . 1986 . Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane . J. Bacteriol. 166 : 244 - 252 . (10.1128/jb.166.1.244-252.1986) / J. Bacteriol. / Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane by Stader J. (1986)
  62. Sterr W. 1995. Diploma thesis. University of Regensburg Regensburg Germany.
  63. Stolz , B. , and H. C. Berg . 1991 . Evidence for interactions between MotA and MotB, torque-generating elements of the flagellar motor of Escherichia coli . J. Bacteriol. 173 : 7033 - 7037 . (10.1128/jb.173.21.7033-7037.1991) / J. Bacteriol. / Evidence for interactions between MotA and MotB, torque-generating elements of the flagellar motor of Escherichia coli by Stolz B. (1991)
  64. Studier , F. W. , and B. A. Moffat . 1986 . Use of bacterial T7 RNA polymerase to direct selective high-level expression of cloned genes . J. Mol. Biol. 189 : 113 - 130 . (10.1016/0022-2836(86)90385-2) / J. Mol. Biol. / Use of bacterial T7 RNA polymerase to direct selective high-level expression of cloned genes by Studier F. W. (1986)
  65. Togashi , F. , S. Yamaguchi , M. Kihara , S. -I. Aizawa , and R. M. Macnab . 1997 . An extreme clockwise switch bias mutation in fliG of Salmonella typhimurium and its suppression by slow-motile mutations in motA and motB . J. Bacteriol. 179 : 2994 - 3003 . (10.1128/jb.179.9.2994-3003.1997) / J. Bacteriol. / An extreme clockwise switch bias mutation in fliG of Salmonella typhimurium and its suppression by slow-motile mutations in motA and motB by Togashi F. (1997)
  66. Trachtenberg , S. , D. J. De Rosier , S. -I. Aizawa , and R. M. Macnab . 1987 . Three-dimensional structure of the complex flagellar filament of Rhizobium lupini and its relation to the structure of the plain filament . J. Mol. Biol. 195 : 603 - 620 . (10.1016/0022-2836(87)90185-9) / J. Mol. Biol. / Three-dimensional structure of the complex flagellar filament of Rhizobium lupini and its relation to the structure of the plain filament by Trachtenberg S. (1987)
  67. Wilson , M. L. , and R. M. Macnab . 1990 . Co-overproduction and localization of the Escherichia coli motility proteins MotA and MotB . J. Bacteriol. 172 : 3932 - 3939 . (10.1128/jb.172.7.3932-3939.1990) / J. Bacteriol. / Co-overproduction and localization of the Escherichia coli motility proteins MotA and MotB by Wilson M. L. (1990)
  68. Yanisch-Perron , C. , J. Vieira , and J. Messing . 1985 . Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors . Gene 33 : 103 - 119 . (10.1016/0378-1119(85)90120-9) / Gene / Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors by Yanisch-Perron C. (1985)
Dates
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Created 8 years, 9 months ago (Nov. 10, 2016, 10:42 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 2:05 p.m.)
Indexed 1 year, 3 months ago (May 15, 2024, 10:22 a.m.)
Issued 27 years, 11 months ago (Oct. 1, 1997)
Published 27 years, 11 months ago (Oct. 1, 1997)
Published Print 27 years, 11 months ago (Oct. 1, 1997)
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@article{Platzer_1997, title={Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti}, volume={179}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.179.20.6391-6399.1997}, DOI={10.1128/jb.179.20.6391-6399.1997}, number={20}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Platzer, J and Sterr, W and Hausmann, M and Schmitt, R}, year={1997}, month=oct, pages={6391–6399} }