Flagellar biogenesis in bacteria is a complex process in which the transcription of dozens of structural and regulatory genes is coordinated with the assembly of the flagellum. Although the overall process of flagellar biogenesis is conserved among bacteria, the mechanisms used to regulate flagellar gene expression vary greatly among different bacterial species. Many bacteria use the alternative sigma factor σ54 (also known as RpoN) to transcribe specific sets of flagellar genes. These bacteria include members of the Epsilonproteobacteria (e.g., Helicobacter pylori and Campylobacter jejuni), Gammaproteobacteria (e.g., Vibrio and Pseudomonas species), and Alphaproteobacteria (e.g., Caulobacter crescentus). This review characterizes the flagellar transcriptional hierarchies in these bacteria and examines what is known about how flagellar gene regulation is linked with other processes including growth phase, quorum sensing, and host colonization. 1. Introduction The flagellum is an exquisitely complex nanomachine that is the primary means for motility in many bacteria. Given that motility plays a vital role in important microbial processes such as chemotaxis, host colonization, and biofilm formation, understanding how bacteria regulate flagellar biogenesis is critical for developing new strategies for the control of harmful microbes and manipulation of useful ones. Flagellar biogenesis is a highly ordered process that involves the coordinated regulation of dozens of structural and regulatory genes with the assembly of the flagellum. As expected for choreographing such an intricate process, flagellar biogenesis involves some of the most sophisticated regulatory mechanisms found in microbiology. Although the structure of the flagellum differs slightly between Gram-negative type and Gram-positive type bacteria, in all cases the bacterial flagellum is comprised of three main parts: the basal body, hook, and filament [1]. Components of the basal body are located within or are closely associated with the cell envelope. The basal body consists of several distinct structures, including the C ring, a type III secretion system known as the flagellar protein export apparatus, the flagellar motor, the rod, and rings that anchor the flagellum to the membrane (Figure 1(a)). Both Gram-negative and Gram-positive type bacteria possess MS and P rings, located in the inner membrane and peptidoglycan layer, respectively. Gram-negative type bacteria possess another ring known as the L ring located in the outer membrane. These rings provide support for the rod as it goes
References
[1]
T. Minamino, K. Imada, and K. Namba, “Mechanisms of type III protein export for bacterial flagellar assembly,” Molecular BioSystems, vol. 4, no. 11, pp. 1105–1115, 2008.
[2]
J. L. McMurry, J. W. Murphy, and B. González-Pedrajo, “The FliN-FliH interaction mediates localization of flagellar export ATPase FliI to the C ring complex,” Biochemistry, vol. 45, no. 39, pp. 11790–11798, 2006.
[3]
R. M. Macnab, Ed., Flagella and Motility, ASM Press, 1996.
[4]
T. Minamino, K. Imada, and K. Namba, “Molecular motors of the bacterial flagella,” Current Opinion in Structural Biology, vol. 18, no. 6, pp. 693–701, 2008.
[5]
T. G. Smith and T. R. Hoover, “Deciphering bacterial flagellar gene regulatory networks in the genomic era,” Advances in Applied Microbiology, vol. 67, pp. 257–295, 2009.
[6]
J. K. Anderson, T. G. Smith, and T. R. Hoover, “Sense and sensibility: flagellum-mediated gene regulation,” Trends in Microbiology, vol. 18, no. 1, pp. 30–37, 2010.
[7]
J. D. Helmann, “Alternative sigma factors and the regulation of flagellar gene expression,” Molecular Microbiology, vol. 5, no. 12, pp. 2875–2882, 1991.
[8]
D. L. Popham, D. Szeto, J. Keener, and S. Kustu, “Function of a bacterial activator protein that binds to transcriptional enhancers,” Science, vol. 243, no. 4891, pp. 629–635, 1989.
[9]
S. Sasse-Dwight and J. D. Gralla, “Probing the Escherichia coliglnALG upstream activation mechanism in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 23, pp. 8934–8938, 1988.
[10]
M. Kihara, T. Minamino, S. Yamaguchi, and R. M. Macnab, “Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus,” Journal of Bacteriology, vol. 183, no. 5, pp. 1655–1662, 2001.
[11]
J. S. van Arnam, J. L. McMurry, M. Kihara, and R. M. Macnab, “Analysis of an engineered Salmonella flagellar fusion protein, FliR-FlhB,” Journal of Bacteriology, vol. 186, no. 8, pp. 2495–2498, 2004.
[12]
C. S. Barker, I. V. Meshcheryakova, A. S. Kostyukova, and F. A. Samatey, “FliO regulation of FliP in the formation of the Salmonella enterica flagellum,” PLoS Genetics, vol. 6, no. 9, Article ID e1001143, 2010.
[13]
A. C. Lowenthal, M. Hill, L. K. Sycuro, K. Mehmood, N. R. Salama, and K. M. Ottemann, “Functional analysis of the Helicobacter pylori flagellar switch proteins,” Journal of Bacteriology, vol. 191, no. 23, pp. 7147–7156, 2009.
[14]
R. M. Macnab, “Type III flagellar protein export and flagellar assembly,” Biochimica et Biophysica Acta, vol. 1694, no. 1–3, pp. 207–217, 2004.
[15]
K. A. Eaton, D. R. Morgan, and S. Krakowka, “Campylobacter pylori virulence factors in gnotobiotic piglets,” Infection and Immunity, vol. 57, no. 4, pp. 1119–1125, 1989.
[16]
K. A. Eaton, D. R. Morgan, and S. Krakowka, “Motility as a factor in the colonisation of gnotobiotic piglets by Helicobacter pylori,” Journal of Medical Microbiology, vol. 37, no. 2, pp. 123–127, 1992.
[17]
D. G. Newell, H. McBride, and J. M. Dolby, “Investigations on the role of flagella in the colonization of infant mice with Campylobacter jejuni and attachment of Campylobacter jejuni to human epithelial cell lines,” Journal of Hygiene, vol. 95, no. 2, pp. 217–227, 1985.
[18]
T. Morooka, A. Umeda, and K. Amako, “Motility as an intestinal colonization factor for Campylobacter jejuni,” Journal of General Microbiology, vol. 131, no. 8, pp. 1973–1980, 1985.
[19]
C. Y. Kao, B. S. Sheu, S. M. Sheu et al., “Higher motility enhances bacterial density and inflammatory response in dyspeptic patients infected with Helicobacter pylori,” Helicobacter, vol. 17, no. 6, pp. 411–416, 2012.
[20]
E. Niehus, H. Gressmann, F. Ye et al., “Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori,” Molecular Microbiology, vol. 52, no. 4, pp. 947–961, 2004.
[21]
M. Balaban, S. N. Joslin, and D. R. Hendrixson, “FlhF and its GTPase activity are required for distinct processes in flagellar gene regulation and biosynthesis in Campylobacter jejuni,” Journal of Bacteriology, vol. 191, no. 21, pp. 6602–6611, 2009.
[22]
A. Kusumoto, A. Shinohara, H. Terashima, S. Kojima, T. Yakushi, and M. Homma, “Collaboration of FlhF and FlhG to regulate polarflagella number and localization in Vibrio alginolyticus,” Microbiology, vol. 154, no. 5, pp. 1390–1399, 2008.
[23]
A. Kusumoto, K. Kamisaka, T. Yakushi, H. Terashima, A. Shinohara, and M. Homma, “Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus,” Journal of Biochemistry, vol. 139, no. 1, pp. 113–121, 2006.
[24]
B. M. Prü？ and P. Matsumura, “A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division,” Journal of Bacteriology, vol. 178, no. 3, pp. 668–674, 1996.
[25]
B. M. Prü？ and P. Matsumura, “Cell cycle regulation of flagellar genes,” Journal of Bacteriology, vol. 179, no. 17, pp. 5602–5604, 1997.
[26]
G. Spohn and V. Scarlato, “Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog,” Journal of Bacteriology, vol. 181, no. 2, pp. 593–599, 1999.
[27]
M. Schirm, E. C. Soo, A. J. Aubry, J. Austin, P. Thibault, and S. M. Logan, “Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori,” Molecular Microbiology, vol. 48, no. 6, pp. 1579–1592, 2003.
[28]
D. Beier and R. Frank, “Molecular characterization of two-component systems of Helicobacter pylori,” Journal of Bacteriology, vol. 182, no. 8, pp. 2068–2076, 2000.
[29]
P. Brahmachary, M. G. Dashti, J. W. Olson, and T. R. Hoover, “Helicobacter pylori FlgR is an enhancer-independent activator of σ54-RNA polymerase holoenzyme,” Journal of Bacteriology, vol. 186, no. 14, pp. 4535–4542, 2004.
[30]
M. M. S. M. W？sten, J. A. Wagenaar, and J. P. M. van Putten, “The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni,” The Journal of Biological Chemistry, vol. 279, no. 16, pp. 16214–16222, 2004.
[31]
M. Bush and R. Dixon, “The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription,” MicroBiology and Molecular Biology Reviews, vol. 76, no. 3, pp. 497–529, 2012.
[32]
J. Schumacher, N. Joly, M. Rappas, X. Zhang, and M. Buck, “Structures and organisation of AAA+ enhancer binding proteins in transcriptional activation,” Journal of Structural Biology, vol. 156, no. 1, pp. 190–199, 2006.
[33]
S. N. Joslin and D. R. Hendrixson, “Analysis of the Campylobacter jejuni FlgR response regulator suggests integration of diverse mechanisms to activate an NtrC-like protein,” Journal of Bacteriology, vol. 190, no. 7, pp. 2422–2433, 2008.
[34]
J. M. Boll and D. R. Hendrixson, “A specificity determinant for phosphorylation in a response regulator prevents in vivo cross-talk and modification by acetyl phosphate,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 50, pp. 20160–20165, 2011.
[35]
S. Porwollik, B. Noonan, and P. W. O'Toole, “Molecular characterization of a flagellar export locus of Helicobacter pylori,” Infection and Immunity, vol. 67, no. 5, pp. 2060–2070, 1999.
[36]
E. Allan, N. Dorrell, S. Foynes, M. Anyim, and B. W. Wren, “Mutational analysis of genes encoding the early flagellar components of Helicobacter pylori: evidence for transcriptional regulation of flagellin A biosynthesis,” Journal of Bacteriology, vol. 182, no. 18, pp. 5274–5277, 2000.
[37]
T. G. Smith, L. Pereira, and T. R. Hoover, “Helicobacter pylori FlhB processing-deficient variants affect flagellar assembly but not flagellar gene expression,” Microbiology, vol. 155, no. 4, pp. 1170–1180, 2009.
[38]
D. R. Hendrixson, B. J. Akerley, and V. J. DiRita, “Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility,” Molecular Microbiology, vol. 40, no. 1, pp. 214–224, 2001.
[39]
J. Tsang, T. G. Smith, L. E. Pereira, and T. R. Hoover, “Insertion mutations in Helicobacter pylori flhA reveal strain differences in RpoN-dependent gene expression,” Microbiology, vol. 159, part 1, pp. 58–67, 2013.
[40]
J. M. Boll and D. R. Hendrixson, “A regulatory checkpoint during flagellar biogenesis in Campylobacter jejuni initiates signal transduction to activate transcription of flagellar genes,” MBio, vol. 4, no. 5, Article ID e00432-13, 2013.
[41]
T. Minamino, H. Doi, and K. Kutsukake, “Substrate specificity switching of the flagellum-specific export apparatus during flagellar morphogenesis in Salmonella typhimurium,” Bioscience, Biotechnology and Biochemistry, vol. 63, no. 7, pp. 1301–1303, 1999.
[42]
M. Erhardt, H. M. Singer, D. H. Wee, J. P. Keener, and K. T. Hughes, “An infrequent molecular ruler controls flagellar hook length in Salmonella enterica,” EMBO Journal, vol. 30, no. 14, pp. 2948–2961, 2011.
[43]
K. T. Hughes, K. L. Gillen, M. J. Semon, and J. E. Karlinsey, “Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator,” Science, vol. 262, no. 5137, pp. 1277–1280, 1993.
[44]
K. A. Ryan, N. Karim, M. Worku, S. A. Moore, C. W. Penn, and P. W. O'Toole, “HP0958 is an essential motility gene in Helicobacter pylori,” FEMS Microbiology Letters, vol. 248, no. 1, pp. 47–55, 2005.
[45]
L. Pereira and T. R. Hoover, “Stable accumulation of σ54 in Helicobacter pylori requires the novel protein HP0958,” Journal of Bacteriology, vol. 187, no. 13, pp. 4463–4469, 2005.
[46]
J. C. Rain, L. Selig, H. de Reuse et al., “The protein-protein interaction map of Helicobacter pylori,” Nature, vol. 409, no. 6817, pp. 211–215, 2001.
[47]
F. P. Douillard, K. A. Ryan, D. L. Caly et al., “Posttranscriptional regulation of flagellin synthesis in Helicobacter pylori by the RpoN chaperone HP0958,” Journal of Bacteriology, vol. 190, no. 24, pp. 7975–7984, 2008.
[48]
C. Josenhans, E. Niehus, S. Amersbach et al., “Functional characterization of the antagonistic flagellar late regulators FliA and FlgM of Helicobacter pylori and their effects on the H. pylori transcriptome,” Molecular Microbiology, vol. 43, no. 2, pp. 307–322, 2002.
[49]
M. Rust, S. Borchert, E. Niehus et al., “The Helicobacter pylori anti-sigma factor FlgM is predominantly cytoplasmic and cooperates with the flagellar basal body protein FlhA,” Journal of Bacteriology, vol. 191, no. 15, pp. 4824–4834, 2009.
[50]
D. R. Hendrixson and V. J. DiRita, “Transcription of σ54-dependent but not σ28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus,” Molecular Microbiology, vol. 50, no. 2, pp. 687–702, 2003.
[51]
M. M. S. M. W？sten, L. van Dijk, A. K. J. Veenendaal, M. R. de Zoete, N. M. C. Bleumink-Pluijm, and J. P. M. van Putten, “Temperature-dependent FlgM/FliA complex formation regulates Campylobacter jejuni flagella length,” Molecular Microbiology, vol. 75, no. 6, pp. 1577–1591, 2010.
[52]
M. G. Prouty, N. E. Correa, and K. E. Klose, “The novel σ54- and σ28-dependent flagellar gene transcription hierarchy of Vibrio cholerae,” Molecular Microbiology, vol. 39, no. 6, pp. 1595–1609, 2001.
[53]
D. Srivastava, M. L. Hsieh, A. Khataokar, M. B. Neiditch, and C. M. Waters, “Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production,” Molecular Microbiology, vol. 90, no. 6, pp. 1262–1276, 2013.
[54]
N. E. Correa, C. M. Lauriano, R. McGee, and K. E. Klose, “Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization,” Molecular Microbiology, vol. 35, no. 4, pp. 743–755, 2000.
[55]
N. E. Correa, J. R. Barker, and K. E. Klose, “The Vibrio cholerae FlgM homologue is an anti-σ28 factor that is secreted through the sheathed polar flagellum,” Journal of Bacteriology, vol. 186, no. 14, pp. 4613–4619, 2004.
[56]
M. Moisi, C. Jenul, S. M. Butler et al., “A novel regulatory protein involved in motility of Vibrio cholerae,” Journal of Bacteriology, vol. 191, no. 22, pp. 7027–7038, 2009.
[57]
L. Aravind and C. P. Ponting, “The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins,” FEMS Microbiology Letters, vol. 176, no. 1, pp. 111–116, 1999.
[58]
S. Merino, J. G. Shaw, and J. M. Tomás, “Bacterial lateral flagella: an inducible flagella system,” FEMS Microbiology Letters, vol. 263, no. 2, pp. 127–135, 2006.
[59]
L. L. McCarter, “Dual flagellar systems enable motility under different circumstances,” Journal of Molecular Microbiology and Biotechnology, vol. 7, no. 1-2, pp. 18–29, 2004.
[60]
S. Ulitzur, “Induction of swarming in Vibrio parahaemolyticus,” Archives of Microbiology, vol. 101, no. 4, pp. 357–363, 1974.
[61]
K. S. Park, M. Arita, T. Iida, and T. Honda, “vpaH, a gene encoding a novel histone-like nucleoid structure-like protein that was possibly horizontally acquired, regulates the biogenesis of lateral flagella in trh-positive Vibrio parahaemolyticus TH3996,” Infection and Immunity, vol. 73, no. 9, pp. 5754–5761, 2005.
[62]
L. McCarter and M. Silverman, “Iron regulation of swarmer cell differentiation of Vibrio parahaemolyticus,” Journal of Bacteriology, vol. 171, no. 2, pp. 731–736, 1989.
[63]
B. J. Stewart and L. L. McCarter, “Lateral flagellar gene system of Vibrio parahaemolyticus,” Journal of Bacteriology, vol. 185, no. 15, pp. 4508–4518, 2003.
[64]
C. J. Gode-Potratz, R. J. Kustusch, P. J. Breheny, D. S. Weiss, and L. L. McCarter, “Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence,” Molecular Microbiology, vol. 79, no. 1, pp. 240–263, 2011.
[65]
J. L. Veesenmeyer, A. R. Hauser, T. Lisboa, and J. Rello, “Pseudomonas aeruginosa virulence and therapy: evolving translational strategies,” Critical Care Medicine, vol. 37, no. 5, pp. 1777–1786, 2009.
[66]
D. Balasubramanian, L. Schneper, H. Kumari, and K. Mathee, “A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence,” Nucleic Acids Research, vol. 41, no. 1, pp. 1–20, 2013.
[67]
T. C. Montie, D. D. Huntzinger, R. C. Craven, and I. A. Holder, “Loss of virulence associated with absence of flagellum in an isogenic mutant of Pseudomonas aeruginosa in the burned-mouse model,” Infection and Immunity, vol. 38, no. 3, pp. 1296–1298, 1982.
[68]
Y. R. Patankar, R. R. Lovewell, M. E. Poynter, J. Jyot, B. I. Kazmierczak, and B. Berwin, “Flagellar motility is a key determinant of the magnitude of the inflammasome response to Pseudomonas aeruginosa,” Infection and Immunity, vol. 81, no. 6, pp. 2043–2052, 2013.
[69]
G. A. O'Toole and R. Kolter, “Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development,” Molecular Microbiology, vol. 30, no. 2, pp. 295–304, 1998.
[70]
K. B. Barken, S. J. Pamp, L. Yang et al., “Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms,” Environmental Microbiology, vol. 10, no. 9, pp. 2331–2343, 2008.
[71]
M. Leeman, J. A. van Pelt, F. M. den Ouden, M. Heinsbroek, P. A. Bakker, and B. Schippers, “Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens,” Phytopathology, vol. 85, no. 9, pp. 1021–1027, 1995.
[72]
P. Hsueh, L. Teng, H. Pan et al., “Outbreak of Pseudomonas fluorescens bacteremia among oncology patients,” Journal of Clinical Microbiology, vol. 36, no. 10, pp. 2914–2917, 1998.
[73]
V. Wong, K. Levi, B. Baddal, J. Turton, and T. C. Boswell, “Spread of Pseudomonas fluorescens due to contaminated drinking water in a bone marrow transplant unit,” Journal of Clinical Microbiology, vol. 49, no. 6, pp. 2093–2096, 2011.
[74]
J. W. Hickman and C. S. Harwood, “Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor,” Molecular Microbiology, vol. 69, no. 2, pp. 376–389, 2008.
[75]
N. Dasgupta, M. C. Wolfgang, A. L. Goodman et al., “A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa,” Molecular Microbiology, vol. 50, no. 3, pp. 809–824, 2003.
[76]
S. K. Arora, B. W. Ritchings, E. C. Almira, S. Lory, and R. Ramphal, “A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner,” Journal of Bacteriology, vol. 179, no. 17, pp. 5574–5581, 1997.
[77]
N. Dasgupta and R. Ramphal, “Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa,” Journal of Bacteriology, vol. 183, no. 22, pp. 6636–6644, 2001.
[78]
N. Dasgupta, S. K. Arora, and R. Ramphal, “fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa,” Journal of Bacteriology, vol. 182, no. 2, pp. 357–364, 2000.
[79]
J. Malakooti and B. Ely, “Principal sigma subunit of the Caulobacter crescentus RNA polymerase,” Journal of Bacteriology, vol. 177, no. 23, pp. 6854–6860, 1995.
[80]
M. T. Laub, H. H. McAdams, T. Feldblyum, C. M. Fraser, and L. Shapiro, “Global analysis of the genetic network controlling a bacterial cell cycle,” Science, vol. 290, no. 5499, pp. 2144–2148, 2000.
[81]
A. K. Benson, G. Ramakrishnan, N. Ohta, J. Feng, A. J. Ninfa, and A. Newton, “The Caulobacter crescentus FlbD protein acts at ftr sequence elements both to activate and to repress transcription of cell cycle-regulated flagellar genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 11, pp. 4989–4993, 1994.
[82]
D. A. Mullin, S. M. van Way, C. A. Blankenship, and A. H. Mullin, “FlbD has a DNA-binding activity near its carboxy terminus that recognizes ftr sequences involved in positive and negative regulation of flagellar gene transcription in Caulobacter crescentus,” Journal of Bacteriology, vol. 176, no. 19, pp. 5971–5981, 1994.
[83]
R. J. Dutton, Z. Xu, and J. W. Gober, “Linking structural assembly to gene expression: a novel mechanism for regulating the activity of a σ54 transcription factor,” Molecular Microbiology, vol. 58, no. 3, pp. 743–757, 2005.
[84]
R. E. Muir, J. Easter, and J. W. Gober, “The trans-acting flagellar regulatory proteins, FliX and FlbD, play a central role in linking flagellar biogenesis and cytokinesis in Caulobacter crescentus,” Microbiology, vol. 151, no. 11, pp. 3699–3711, 2005.
[85]
P. E. Anderson and J. W. Gober, “FlbT, the post-transcriptional regulator of flagellin synthesis in Caulobacter crescentus, interacts with the 5′ untranslated region of flagellin mRNA,” Molecular Microbiology, vol. 38, no. 1, pp. 41–52, 2000.
[86]
A. T. Nielsen, N. A. Dolganov, G. Otto, M. C. Miller, C. Y. Wu, and G. K. Schoolnik, “RpoS controls the Vibrio cholerae mucosal escape response,” PLoS Pathogens, vol. 2, no. 10, article e109, 2006.
[87]
M. T. Laub, S. L. Chen, L. Shapiro, and H. H. McAdams, “Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 7, pp. 4632–4637, 2002.
[88]
A. J. Kelly, M. J. Sackett, N. Din, E. Quardokus, and Y. V. Brun, “Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter,” Genes and Development, vol. 12, no. 6, pp. 880–893, 1998.
[89]
M. Wortinger, M. J. Sackett, and Y. V. Brun, “CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus,” EMBO Journal, vol. 19, no. 17, pp. 4503–4512, 2000.
[90]
R. E. Muir, T. M. O'Brien, and J. W. Gober, “The Caulobacter crescentus flagellar gene, fliX, encodes a novel trans-acting factor that couples flagellar assembly to transcription,” Molecular Microbiology, vol. 39, no. 6, pp. 1623–1637, 2001.
[91]
M. Llewellyn, R. J. Dutton, J. Easter, D. O'Donnol, and J. W. Gober, “The conserved flaF gene has a critical role in coupling flagellin translation and assembly in Caulobacter crescentus,” Molecular Microbiology, vol. 57, no. 4, pp. 1127–1142, 2005.
[92]
S. M. Kim, D. H. Lee, and S. H. Choi, “Evidence that the Vibrio vulnificus flagellar regulator FlhF is regulated by a quorum sensing master regulator SmcR,” Microbiology, vol. 158, part 8, pp. 2017–2025, 2012.
[93]
F. Martínez-Granero, A. Navazo, E. Barahona, M. Redondo-Nieto, R. Rivilla, and M. Martín, “The Gac-Rsm and SadB signal transduction pathways converge on Algu to downregulate motility in Pseudomonas fluorescens,” PLoS ONE, vol. 7, no. 2, Article ID e31765, 2012.
[94]
C. Reimmann, M. Beyeler, A. Latifi et al., “The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase,” Molecular Microbiology, vol. 24, no. 2, pp. 309–319, 1997.
[95]
J. Dubern and G. V. Bloemberg, “Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445,” FEMS Microbiology Letters, vol. 263, no. 2, pp. 169–175, 2006.
[96]
M. G. Surette, M. B. Miller, and B. L. Bassler, “Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 4, pp. 1639–1644, 1999.
[97]
B. A. Rader, S. R. Campagna, M. F. Semmelhack, B. L. Bassler, and K. Guillemin, “The quorum-sensing molecule autoinducer 2 regulates motility and flagellar morphogenesis in Helicobacter pylori,” Journal of Bacteriology, vol. 189, no. 17, pp. 6109–6117, 2007.
[98]
Y. He, J. G. Frye, T. P. Strobaugh Jr., and C. Chen, “Analysis of AI-2/LuxS-dependent transcription in Campylobacter jejuni strain 81-176,” Foodborne Pathogens and Disease, vol. 5, no. 4, pp. 399–415, 2008.
[99]
B. Jeon, K. Itoh, N. Misawa, and S. Ryu, “Effects of quorum sensing on flaA transcription and autoagglutination in Campylobacter jejuni,” Microbiology and Immunology, vol. 47, no. 11, pp. 833–839, 2003.
[100]
N. Dasgupta, E. P. Ferrell, K. J. Kanack, S. E. H. West, and R. Ramphal, “fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is σ70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein,” Journal of Bacteriology, vol. 184, no. 19, pp. 5240–5250, 2002.
[101]
J. Zhu, M. B. Miller, R. E. Vance, M. Dziejman, B. L. Bassler, and J. J. Mekalanos, “Quorum-sensing regulators control virulence gene expression in Vibrio cholerae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 5, pp. 3129–3134, 2002.
[102]
Z. Liu, T. Miyashiro, A. Tsou, A. Hsiao, M. Goulian, and J. Zhu, “Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 28, pp. 9769–9774, 2008.
[103]
K. E. Klose, V. Novik, and J. J. Mekalanos, “Identification of multiple σ54-dependent transcriptional activators in Vibrio cholerae,” Journal of Bacteriology, vol. 180, no. 19, pp. 5256–5259, 1998.
[104]
I. Kawagishi, M. Imagawa, Y. Imae, L. McCarter, and M. Homma, “The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression,” Molecular Microbiology, vol. 20, no. 4, pp. 693–699, 1996.
[105]
T. J. Kirn, B. A. Jude, and R. K. Taylor, “A colonization factor links Vibrio cholerae environmental survival and human infection,” Nature, vol. 438, no. 7069, pp. 863–866, 2005.
[106]
Z. Kuang, Y. Hao, S. Hwang et al., “The Pseudomonas aeruginosa flagellum confers resistance to pulmonary surfactant protein-A by impacting the production of exoproteases through quorum-sensing,” Molecular Microbiology, vol. 79, no. 5, pp. 1220–1235, 2011.
[107]
S. Zhang, F. X. McCormack, R. C. Levesque, G. A. O'Toole, and G. W. Lau, “The flagellum of Pseudomonas aeruginosa is required for resistance to clearance by surfactant protein A,” PLoS ONE, vol. 2, no. 6, article e564, 2007.
[108]
G. W. Lau, D. J. Hassett, H. Ran, and F. Kong, “The role of pyocyanin in Pseudomonas aeruginosa infection,” Trends in Molecular Medicine, vol. 10, no. 12, pp. 599–606, 2004.
[109]
G. W. Lau, H. Ran, F. Kong, D. J. Hassett, and D. Mavrodi, “Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice,” Infection and Immunity, vol. 72, no. 7, pp. 4275–4278, 2004.
[110]
D. S. Merrell, M. L. Goodrich, G. Otto, L. S. Tompkins, and S. Falkow, “pH-regulated gene expression of the gastric pathogen Helicobacter pylori,” Infection and Immunity, vol. 71, no. 6, pp. 3529–3539, 2003.
[111]
K. J. Allen and M. W. Griffiths, “Effect of environmental and chemotactic stimuli on the activity of the Campylobacter jejuni flaAσ28 promoter,” FEMS Microbiology Letters, vol. 205, no. 1, pp. 43–48, 2001.
[112]
Y. Wen, J. Feng, D. R. Scott, E. A. Marcus, and G. Sachs, “The pH-responsive regulon of HP0244 (FlgS), the cytoplasmic histidine kinase of Helicobacter pylori,” Journal of Bacteriology, vol. 191, no. 2, pp. 449–460, 2009.
[113]
D. R. Hendrixson, “A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism,” Molecular Microbiology, vol. 61, no. 6, pp. 1646–1659, 2006.
[114]
D. R. Hendrixson, “Restoration of flagellar biosynthesis by varied mutational events in Campylobacter jejuni,” Molecular Microbiology, vol. 70, no. 2, pp. 519–536, 2008.
[115]
P. Lertsethtakarn, K. M. Ottemann, and D. R. Hendrixson, “Motility and chemotaxis in Campylobacter and Helicobacter,” Annual Review of Microbiology, vol. 65, pp. 389–410, 2011.
[116]
S. F. Park, D. Purdy, and S. Leach, “Localized reversible frameshift mutation in the flhA gene confers phase variability to flagellin gene expression in Campylobacter coli,” Journal of Bacteriology, vol. 182, no. 1, pp. 207–210, 2000.
[117]
C. Josenhans, K. A. Eaton, T. Thevenot, and S. Suerbaum, “Switching of flagellar motility in Helicobacter pylori by reversible length variation of a short homopolymeric sequence repeat in fliP, a gene encoding a basal body protein,” Infection and Immunity, vol. 68, no. 8, pp. 4598–4603, 2000.
[118]
N. de Vries, D. Duinsbergen, E. J. Kuipers et al., “Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori,” Journal of Bacteriology, vol. 184, no. 23, pp. 6615–6623, 2002.
[119]
Y. N. Srikhanta, R. J. Gorrell, J. A. Steen et al., “Phasevarion mediated epigenetic gene regulation in Helicobacter pylori,” PLoS ONE, vol. 6, no. 12, Article ID e27569, 2011.
[120]
K. L. Fox, Y. N. Srikhanta, and M. P. Jennings, “Phase variable type III restriction-modification systems of host-adapted bacterial pathogens,” Molecular Microbiology, vol. 65, no. 6, pp. 1375–1379, 2007.
[121]
S. K. Lee, A. Stack, E. Katzowitsch, S. I. Aizawa, S. Suerbaum, and C. Josenhans, “Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5,” Microbes and Infection, vol. 5, no. 15, pp. 1345–1356, 2003.
[122]
L. F. Lin, J. Posfai, R. J. Roberts, and H. Kong, “Comparative genomics of the restriction-modification systems in Helicobacter pylori,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 5, pp. 2740–2745, 2001.
[123]
Y. Zheng, J. Posfai, R. D. Morgan, T. Vincze, and R. J. Roberts, “Using shotgun sequence data to find active restriction enzyme genes,” Nucleic Acids Research, vol. 37, no. 1, article e1, 2009.
[124]
R. Kumar, A. K. Mukhopadhyay, P. Ghosh, and D. N. Rao, “Comparative transcriptomics of H. pylori strains AM5, SS1 and their hpyAVIBM deletion mutants: possible roles of cytosine methylation,” PLoS ONE, vol. 7, no. 8, Article ID e42303, 2012.
[125]
E. Déziel, Y. Comeau, and R. Villemur, “Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities,” Journal of Bacteriology, vol. 183, no. 4, pp. 1195–1204, 2001.
[126]
M. Sánchez-Contreras, M. Martín, M. Villacieros, F. O'Gara, I. Bonilla, and R. Rivilla, “Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113,” Journal of Bacteriology, vol. 184, no. 6, pp. 1587–1596, 2002.
[127]
C. M. Sharma, S. Hoffmann, F. Darfeuille et al., “The primary transcriptome of the major human pathogen Helicobacter pylori,” Nature, vol. 464, no. 7286, pp. 250–255, 2010.
