Recruitment of the Earliest Component of the Bacterial Flagellum to the Old Cell Division Pole by a Membrane-Associated Signal Recognition Particle Family GTP-Binding Protein

Green, Johnathan C.D.; Kahramanoglou, Christina; Rahman, A. K. M. Shahidur; Pender, Alexandra; Charbonnel, Nicolas; Fraser, Gillian M.

doi:10.1016/j.jmb.2009.05.075

Cited by 78 publications

(140 citation statements)

References 59 publications

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“…Furthermore, the cell cycle-dependent polar localization of ParC and chemotaxis proteins is independent of FlhF, a protein required for polar positioning of the flagellum (Green et al 2009) and of the flagellar MS ring component FliF (Supplemental Fig. S9), suggesting that the positioning of the flagellar and chemotactic machineries occur through independent pathways.…”

Section: Discussionmentioning

confidence: 99%

A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins

Ringgaard¹,

Schirner²,

Davis³

et al. 2011

Genes Dev.

162

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Stochastic processes are thought to mediate localization of membrane-associated chemotaxis signaling clusters in peritrichous bacteria. Here, we identified a new family of ParA-like ATPases (designated ParC ½for partitioning chemotaxis) encoded within chemotaxis operons of many polar-flagellated g-proteobacteria that actively promote polar localization of chemotaxis proteins. In Vibrio cholerae, a single ParC focus is found at the flagellated old pole in newborn cells, and later bipolar ParC foci develop as the cell matures. The cell cycle-dependent redistribution of ParC occurs by its release from the old pole and subsequent relocalization at the new pole, consistent with a ''diffusion and capture'' model for ParC dynamics. Chemotaxis proteins encoded in the same cluster as ParC have a similar unipolar-to-bipolar transition; however, they reach the new pole after the arrival of ParC. Cells lacking ParC exhibit aberrantly localized foci of chemotaxis proteins, reduced chemotaxis, and altered motility, which likely accounts for their enhanced colonization of the proximal small intestine in an animal model of cholera. Collectively, our findings indicate that ParC promotes the efficiency of chemotactic signaling processes. In particular, ParC-facilitated development of a functional chemotaxis apparatus at the new pole readies this site for its development into a functional old pole after cell division.

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Section: Discussionmentioning

confidence: 99%

A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins

Ringgaard¹,

Schirner²,

Davis³

et al. 2011

Genes Dev.

162

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show abstract

“…For instance, FlhF is required for expression of some 54 -and 28 -dependent flagellar genes and for production of flagella in the classical biotype of Vibrio cholerae (10). However, V. cholerae flhF mutants of another biotype can produce a flagellum in a minority of cells, but the flagellum is at a lateral site (14). Similar lateral flagella were found in flhF mutants of Pseudomonas aeruginosa and Pseudomonas putida (34,37).…”

mentioning

confidence: 83%

FlhF and Its GTPase Activity Are Required for Distinct Processes in Flagellar Gene Regulation and Biosynthesis in Campylobacter jejuni

2009

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“…FlhF is required for the targeting of the first flagellar protein, FliF, to the cell pole 25 by a mechanism that is so far poorly understood. FlhF is associated with the membrane 25,26 and localizes at the cell pole 20 . The FlhF protein (Fig.…”

mentioning

confidence: 99%

Structural basis for the molecular evolution of SRP-GTPase activation by protein

Bange

Kümmerer

Grudnik

et al. 2011

Nat Struct Mol Biol

100

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SIMIBI-class (named after the signal recognition particle, MinD, BioD) nucleotide-binding proteins appeared early in evolution 1 and contain GTPases, as well as ATPases, involved in the correct localization of cellular constituents. The MinD ATPase, as the central part of the Min system, regulates the determination of the cell division site in all bacterial species 2 . SRP-GTPases form a subfamily of the SIMIBI class, with only three members: the signal sequence-binding protein Ffh (SRP54 in Eukarya and Archaea), the SRP receptor FtsY (SR in Eukarya) and FlhF, which is involved in flagella biosynthesis [3][4][5] . They share the conserved NG domain, which contains two major additions to the conserved fold of small G proteins. First, an --element (I-box) is inserted in the effector region; second, the N domain, comprising four -helices, is attached to the N terminus of the G domain. SRP (Ffh together with the SRP RNA) and FtsY constitute the universally conserved co-translational protein-targeting machinery 6,7 . When bound to GTP, Ffh and FtsY form, through interactions between their NG domains 8,9 , a heterodimeric complex that regulates the transfer of a ribosome-nascent chain complex to a vacant translocon in the membrane with a series of conformational rearrangements 10,11 . The two GTPases share a composite active site between their G domains in which GTP hydrolysis is reciprocally activated 12 . The SRP RNA [13][14][15] and membrane lipids 16,17 play fundamental roles in activating the Ffh-FtsY GTPases. The recent structure of the SRP-FtsY complex, together with biochemical implications, suggest that the distal end of the hairpin-like SRP RNA may be involved in this activation 18 . The third SRP-GTPase FlhF, together with the MinD-type protein YlxH (also known as FlhG, FleN, motR or MinD2), is essential for the placement and assembly of flagella 19 in many polar and peritrichous flagellated bacteria [20][21][22][23][24] . FlhF is required for the targeting of the first flagellar protein, FliF, to the cell pole 25 by a mechanism that is so far poorly understood. FlhF is associated with the membrane 25,26 and localizes at the cell pole 20 . The FlhF protein (Fig. 1a) contains an N-terminal B domain that seems to be involved in FliF targeting 25 ; it shares the NG domain fold with the other two members of the SRP-GTPase subfamily. FlhF forms a stable homodimer with GTP and a composite active site that is basically identical to the active site of the Ffh-FtsY heterodimer 5 . In both the homo-and heterodimer, the two nucleotides are bound in a head-to-tail manner, with the -phosphate of one nucleotide interacting with the 3 -OH of the ribose moiety of the other. However, for the homo-and heterodimers formed by the three SRP-GTPases, the molecular mechanism of activation is still unknown. We set out to understand the activation of SRPGTPases by studying FlhF. RESULTS The SRP-GTPase FlhF is activated by YlxHAs FlhF (Fig. 1) forms a stable homodimer, and reciprocal activation has not been observed 5 , we reasoned ...

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Recruitment of the Earliest Component of the Bacterial Flagellum to the Old Cell Division Pole by a Membrane-Associated Signal Recognition Particle Family GTP-Binding Protein

Cited by 78 publications

References 59 publications

A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins

A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins

FlhF and Its GTPase Activity Are Required for Distinct Processes in Flagellar Gene Regulation and Biosynthesis in Campylobacter jejuni

Structural basis for the molecular evolution of SRP-GTPase activation by protein

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