FlhE functions as a chaperone to prevent formation of periplasmic flagella in Gram-negative bacteria

• Published in: Nature communications 2024-07, Vol.15 (1), p.5921-15, Article 5921
• Main Authors: Halte, Manuel, Andrianova, Ekaterina P., Goosmann, Christian, Chevance, Fabienne F. V., Hughes, Kelly T., Zhulin, Igor B., Erhardt, Marc
• Format: Article
• Language: English
• Subjects: 14/19; 14/28; 14/34; 38/35; 631/326/1320; 631/326/41/1969/2180; 631/326/88; 96/63; Assembly; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Cell morphology; Cell walls; Control rods; Flagella; Flagella - genetics; Flagella - metabolism; Flagella - ultrastructure; Gene expression; Gene Expression Regulation, Bacterial; Gram-negative bacteria; Humanities and Social Sciences; Lysis; Microscopy; Microscopy, Electron, Transmission; Molecular Chaperones - genetics; Molecular Chaperones - metabolism; Molecular structure; Morphogenesis; Morphology; Motility; multidisciplinary; Periplasm; Periplasm - metabolism; Periplasmic Proteins - genetics; Periplasmic Proteins - metabolism; Protein biosynthesis; Protein structure; Proteins; Rotors; Salmonella enterica - genetics; Salmonella enterica - metabolism; Science; Science (multidisciplinary); Stators; Structural proteins; Transmission electron microscopy
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-50278-0

The bacterial flagellum, which facilitates motility, is composed of ~20 structural proteins organized into a long extracellular filament connected to a cytoplasmic rotor-stator complex via a periplasmic rod. Flagellum assembly is regulated by multiple checkpoints that ensure an ordered gene expression pattern coupled to the assembly of the various building blocks. Here, we use epifluorescence, super-resolution, and transmission electron microscopy to show that the absence of a periplasmic protein (FlhE) prevents proper flagellar morphogenesis and results in the formation of periplasmic flagella in Salmonella enterica . The periplasmic flagella disrupt cell wall synthesis, leading to a loss of normal cell morphology resulting in cell lysis. We propose that FlhE functions as a periplasmic chaperone to control assembly of the periplasmic rod, thus preventing formation of periplasmic flagella. The bacterial flagellum is a complex macromolecular structure that requires a highly regulated assembly of building blocks. Here, Halte et al. show that a protein controls assembly of the flagellum’s periplasmic rod and prevents misformation of flagella in the periplasm.