Caulobacter FliQ and FliR membrane proteins, required for flagellar biogenesis and cell division, belong to a family of virulence factor export proteins

Abstract

Each Caulobacter crescentus cell division generates distinct progeny cells: a stalked cell which is competent for DNA replication, and a motile swarmer cell which initiates DNA replication only after it sheds its flagellum and differentiates into a stalked cell later in the cell cycle. Following the initiation of DNA replication, the flagellar transcriptional hierarchy is activated, culminating in the assembly of a single flagellum at the cell pole opposite that bearing the stalk. The biogenesis of the flagellum is a landmark in the establishment of asymmetry in the predivisional cell (Fig. 1).A large number of the flagellar structural and regulatory genes have been grouped into classes (Fig. 1) that form a regulatory hierarchy (7,9,11,43,62). We have preliminary evidence that the class I genes respond to cell cycle cues (44a). The class II flagellar genes are transcribed early in the cell cycle and are required for the transcription of genes in classes III and IV. Two class II genes, rpoN and flbD, encode a sigma factor ( 54 ) (6), and a transcriptional activator, FlbD (45, 60), respectively, which are required directly for the transcription of class III and class IV genes. Other class II genes encode proteins required for flagellar assembly and function (24, 45a, 65). The order of flagellar gene expression approximates the order of assembly of the gene products into the nascent structure (11,13,17,43,62). In C. crescentus, Salmonella typhimurium, and Escherichia coli, if flagellar assembly is aborted, transcription of the remaining flagellar genes is blocked, suggesting that the two processes are coupled (19,23,24,31).We reported previously that a nonmotile mutant with a deletion in the flaS locus not only diminished or abolished the transcription of class III and class IV genes but also exhibited a cell division defect (13). To understand the role of this class II flaS locus in the assembly of the flagellum and in cell divi- At each division, a predivisional cell gives rise to two different progeny, a stalked cell and a motile swarmer cell. As the cell cycle proceeds, the swarmer cell sheds its flagellum and assembles a stalk at the previously flagellated pole. The new stalked cell begins to divide, assembling a new flagellum at the pole opposite the stalk. The flagellar genes are expressed in an order that reflects their positions in the regulatory hierarchy and the order of assembly of their protein products into the flagellum (7,42). Arrows indicate positive regulation, such that transcription of each class of genes requires the expression of the gene products of the preceding class. Both rpoN and flbD encode transcription proteins (6, 45), whereas other class II genes appear to encode proteins involved in the assembly, structure, and function of the flagellum (24, 65).

New members of the ctrA regulon: the major chemotaxis operon in Caulobacter is CtrA dependent

“…2d and Fig. 5 (Van Way et al, 1993), fliQp (Zhuang & Shapiro, 1995), flhAp (Ramakrishnan et al, 1991 ;Sanders et al, 1992), fliXp (Mohr et al, 1998) and fliLp (Yu & Shapiro, 1992 that the mcpA promoter is different from other CtrAdependent class II promoters is provided by the finding that transcription of mcpA is inhibited when membrane synthesis is blocked (Brassinga et al, 2000), whilst other flagellar class II promoters are not affected. Finally, although we have been able to obtain a DNase I footprint of the fliQ promoter with CtrA we have been unsuccessful in binding CtrA to the mcpA promoter (S. E. Jones, unpublished).…”

The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body

“…The genetic origins of these proteins were unknown at the time of that study. Subsequently, the fliP and fliR genes have been characterized in several bacterial species (Carpenter et al, 1993;Mulholland et al, 1993;Malakooti et al, 1994;Hardham et al, 1995;Zhuang and Shapiro, 1995;Ge and Charon, 1997;Ohnishi et al, 1997).…”

Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control

“…The unusual consensus sequence of class II promoters suggested that transcription of these genes and thus their temporal pattern of activity is controlled by a novel sigma factor [27,42,43]. However, in vitro activation of class II promoters by the Ec 73 RNA polymerase indicates that these promoters are in fact recognized by the C. crescentus housekeeping sigma factor [44].…”

“…Initiation of £iL and £iF transcription in vitro was dependent on the presence of CtrA in the assay [44]. All CtrA-controlled promoters share a similar architecture with a CtrAbinding site (CtrA-box) overlapping the 335 region [45,46] and with nucleotides in the CtrA-box being essential for their transcriptional activity [27,42]. In vitro binding studies have shown that phosphorylation enhances the a¤nity of CtrA for the £iQ promoter approximately 50-fold [46].…”