A flagellum-specific chaperone facilitates assembly of the core type III export apparatus of the bacterial flagellum

• Published in: PLoS biology 2017-08, Vol.15 (8), p.e2002267-e2002267
• Main Authors: Fabiani, Florian D, Renault, Thibaud T, Peters, Britta, Dietsche, Tobias, Gálvez, Eric J C, Guse, Alina, Freier, Karen, Charpentier, Emmanuelle, Strowig, Till, Franz-Wachtel, Mirita, Macek, Boris, Wagner, Samuel, Hensel, Michael, Erhardt, Marc
• Format: Article
• Language: English
• Subjects: Assembling; Assembly; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biochemistry; Biodegradation; Biology and Life Sciences; Biosynthesis; Exports; Flagella; Flagella - physiology; Flagellates; Funding; Homology; Infections; Kinases; Localization; Machinery; Machinery and equipment; Mass spectrometry; Medicine and Health Sciences; Membrane proteins; Membrane Proteins - genetics; Membrane Proteins - metabolism; Methods; Microscopy; Molecular biology; Molecular chaperones; Phylogeny; Physiological aspects; Protein transport; Proteins; Proteolysis; Proteomics; Protonmotive force; Quality control; Research and Analysis Methods; Salmonella; Scientific imaging; Secretion; Supervision; Type III Secretion Systems; Virulence
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.2002267

Many bacteria move using a complex, self-assembling nanomachine, the bacterial flagellum. Biosynthesis of the flagellum depends on a flagellar-specific type III secretion system (T3SS), a protein export machine homologous to the export machinery of the virulence-associated injectisome. Six cytoplasmic (FliH/I/J/G/M/N) and seven integral-membrane proteins (FlhA/B FliF/O/P/Q/R) form the flagellar basal body and are involved in the transport of flagellar building blocks across the inner membrane in a proton motive force-dependent manner. However, how the large, multi-component transmembrane export gate complex assembles in a coordinated manner remains enigmatic. Specific for most flagellar T3SSs is the presence of FliO, a small bitopic membrane protein with a large cytoplasmic domain. The function of FliO is unknown, but homologs of FliO are found in >80% of all flagellated bacteria. Here, we demonstrate that FliO protects FliP from proteolytic degradation and promotes the formation of a stable FliP-FliR complex required for the assembly of a functional core export apparatus. We further reveal the subcellular localization of FliO by super-resolution microscopy and show that FliO is not part of the assembled flagellar basal body. In summary, our results suggest that FliO functions as a novel, flagellar T3SS-specific chaperone, which facilitates quality control and productive assembly of the core T3SS export machinery.