Type III secretion systems and bacterial flagella: Insights into their function from structural similarities

Blocker, Ariel; Komoriya, Kaoru; Aizawa, Shin‐Ichi

doi:10.1073/pnas.0535335100

Cited by 275 publications

(243 citation statements)

References 76 publications

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“…Its original role as a secretion apparatus is also supported by the clear links between the flagellum and the TTSS, a protein delivery system whose genetic architecture is similar to and derived from a flagellar gene complex (17,20). Although some bacterial genomes contain recent paralogs of particular flagellar genes, most flagellar genes originated very early and are highly divergent, which occasionally hampers the recognition of orthologs, or the similarity between core proteins, in some of the genomes that we considered.…”

Section: Discussionmentioning

confidence: 99%

“…Because the flagellar motor proteins MotA/B are homologous to the motor proteins in the Tol-pal and TonB systems (15), the flagellum was hypothesized to have originated as a simple proton-driven secretion system (16). Most significantly, there are well established sequence and structural homologies between bacterial flagella and the type III secretion system (TTSS) demonstrating that the two apparati derive from a common ancestor (17). Most evidence, including their much broader phylogenetic distribution, supports the view that the flagellum arose much earlier that the TTSS, which are largely limited to Proteobacteria (18)(19)(20).…”

Section: Stepwise Formation Of the Bacterial Flagellar Systemmentioning

confidence: 99%

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Stepwise formation of the bacterial flagellar system

Liu

Ochman

2007

Proc. Natl. Acad. Sci. U.S.A.

227

206

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Elucidating the origins of complex biological structures has been one of the major challenges of evolutionary studies. The bacterial flagellum is a primary example of a complex apparatus whose origins and evolutionary history have proven difficult to reconstruct. The gene clusters encoding the components of the flagellum can include >50 genes, but these clusters vary greatly in their numbers and contents among bacterial phyla. To investigate how this diversity arose, we identified all homologs of all flagellar proteins encoded in the complete genome sequences of 41 flagellated species from 11 bacterial phyla. Based on the phylogenetic occurrence and histories of each of these proteins, we could distinguish an ancient core set of 24 structural genes that were present in the common ancestor to all Bacteria. Within a genome, many of these core genes show sequence similarity only to other flagellar core genes, indicating that they were derived from one another, and the relationships among these genes suggest the probable order in which the structural components of the bacterial flagellum arose. These results show that core components of the bacterial flagellum originated through the successive duplication and modification of a few, or perhaps even a single, precursor gene.

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Section: Discussionmentioning

confidence: 99%

Section: Stepwise Formation Of the Bacterial Flagellar Systemmentioning

confidence: 99%

Stepwise formation of the bacterial flagellar system

Liu

Ochman

2007

Proc. Natl. Acad. Sci. U.S.A.

227

206

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“…The bacterial injectisome (or needle complex) is structurally similar to the flagellum and consists of a basal body-like structure, an associated T3SS, and a hollow needle-like filament that protrudes from the cell surface and serves as the conduit through which proteins are secreted [18]. Much like the flagellum, assembly of the injectisome is thought to proceed in a sequential manner starting with formation of a basal structure and ending with T3SS-dependent export of the needle protein to the distal tip [4].…”

Section: Secretory Activity As An Inducing Signal In the Injectisome mentioning

confidence: 99%

Control of gene expression by type III secretory activity

Brutinel

Yahr

2008

Current Opinion in Microbiology

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SummaryThe bacterial flagellum and the highly related injectisome (or needle complex) are among the most complicated multi-protein structures found in Gram-negative microorganisms. The assembly of both structures is dependent upon a type III secretion system. An interesting regulatory feature unique to these systems is the coordination of gene expression with type III secretory activity. This means of regulation ensures that secretion substrates are expressed only when required during the assembly process or upon completion of the fully functional structure. Prominent within the regulatory scheme are secreted proteins and type III secretion chaperones that exert effects on gene expression at the transcriptional and post-transcriptional levels. Although the major structural components of the flagellum and injectisome systems are highly conserved, recent studies reveal diversity in the mechanisms used by secretion substrates and chaperones to control gene expression.

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“…This apparatus is related to the injectisome used by many gram-negative pathogens and symbionts to transfer effector proteins into host cells; in both systems this export mechanism is termed 'type III' secretion 2,3 . The flagellar secretion apparatus comprises a membrane-embedded complex of about five proteins, and soluble factors, which include export-dedicated chaperones and an ATPase, FliI, that was thought to provide the energy for export 1,4 .…”

mentioning

confidence: 99%

Energy source of flagellar type III secretion

Paul

Erhardt

Hirano

et al. 2008

Nature

293

317

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Bacterial flagella contain a specialized secretion apparatus that functions to deliver the protein subunits that form the filament and other structures to outside the membrane 1 . This apparatus is related to the injectisome used by many gram-negative pathogens and symbionts to transfer effector proteins into host cells; in both systems this export mechanism is termed 'type III' secretion 2,3 . The flagellar secretion apparatus comprises a membrane-embedded complex of about five proteins, and soluble factors, which include export-dedicated chaperones and an ATPase, FliI, that was thought to provide the energy for export 1,4 . Here we show that flagellar secretion in Salmonella enterica requires the proton motive force (PMF) and does not require ATP hydrolysis by FliI. The export of several flagellar export substrates was prevented by treatment with the protonophore CCCP, with no accompanying decrease in cellular ATP levels. Weak swarming motility and rare flagella were observed in a mutant deleted for FliI and for the nonflagellar type-III secretion ATPases InvJ and SsaN. These findings show that the flagellar secretion apparatus functions as a protondriven protein exporter and that ATP hydrolysis is not essential for type III secretion.Flagellar assembly begins with structures in the cytoplasmic membrane and proceeds through steps that add the exterior structures in a proximal-to-distal sequence (Fig. 1) 1 . Assembly of the rod, hook and filament requires the action of the secretion apparatus, which transports the needed subunits into a central channel through the structure that conducts them to their site of incorporation at the tip ( Fig. 1). Flagellar export is notably fast: in the early stages of filament growth flagellin is delivered at a rate of several 55 kDa subunits per second 5 .ATP hydrolysis by FliI was thought to provide the energy for export because mutations that delete or reduce the activity of FliI block flagellar synthesis at the stage of rod assembly 1,4,6 (Fig. 1). Homologues of FliI also occur in the type III secretion apparatus of injectisomes and are usually assumed to energize export in those systems as well. Some evidence for a different view has also been reported: it was observed that type III secretion in Yersinia enterocolitica was prevented by the protonophore CCCP 7 , and it was shown that the secretion ATPase InvC of Salmonella functions to dissociate export substrate from the chaperone 8 , a role distinct from transport itself. The energy source for type III secretion thus remains uncertain.To address the energy requirements for type III secretion, we first measured the effect of the uncoupler CCCP on flagellar export in S. enterica, assayed by accumulation of the export substrate FlgM in the medium. FlgM export was prevented by 10 mM or more CCCP (Fig. 2a). Overall cellular energy levels seemed unaffected, because cells grew normally in 10 mM CCCP (growth data not shown) and ATP levels were unchanged ( Supplementary Fig. 1). The effect was reversible: FlgM export was largely re...

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Type III secretion systems and bacterial flagella: Insights into their function from structural similarities

Abstract: Type III secretion systems and bacterial flagella are broadly compared at the level of their genetic structure, morphology, regulation, and function, integrating structural information, to provide an overview of how they might function at a molecular level.

Cited by 275 publications

References 76 publications

Stepwise formation of the bacterial flagellar system

Stepwise formation of the bacterial flagellar system

Control of gene expression by type III secretory activity

Energy source of flagellar type III secretion

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