Transcriptional and functional characterizations of multiple flagellin genes in spirochetes. Issue 3 (18th July 2022)

• Record Type: Journal Article
• Authors: Kurniyati, Kurni; Chang, Yunjie; Liu, Jun; Li, Chunhao
• Is Part Of: Molecular microbiology. Volume 118:Issue 3(2022)
• Page Start: 175
• Page End: 190
• Publication Date: 2022-07-18
• Subjects: motility -- flagellin -- sigma factors -- spirochetes -- Treponema; Molecular microbiology -- Periodicals; 572.829
• DOI: 10.1111/mmi.14959
• Languages: English
• ISSNs: 0950-382X

Abstract

Abstract: The flagellar filament is a helical propeller for bacterial locomotion. In external flagellates, the filaments are mostly homopolymers of a single flagellin protein. By contrast, the flagellar filaments of spirochetes are mostly heteropolymers of multiple flagellin proteins. This report seeks to investigate the role of multiple flagellin proteins using the oral spirochete Treponema denticola as a model. First, biochemical and genetic studies uncover that the flagellar filaments of T. denticola mainly comprise four proteins, FlaA, FlaB1, FlaB2, and FlaB3, in a defined stoichiometry. Second, transcriptional analyses reveal that the genes encoding these four proteins are regulated by two different transcriptional factors, sigma 28 and sigma 70 . Third, loss‐of‐function studies demonstrate that each individual flagellin protein contributes to spirochete motility, but none of them is absolutely required. Last, we provide genetic and structural evidence that FlaA forms a "seam"‐like structure around the core and that deletion of individual flagellin protein alters the flagellar homeostasis. Collectively, these results demonstrate that T. denticola has evolved a unique mechanism to finely regulate its flagellar filament gene expression and assembly which renders the organelle with the right number, shape, strength, and structure for its distinct motility. Abstract : The oral spirochete Treponema denticola has periplasmic flagella (PFs) that are mainly composed of three flagellin proteins (FlaB1, FlaB2 and FlaB3) and a sheath protein FlaA. Each protein contributes to the motility but none of them is absolutely required. Structurally, FlaB proteins form a core (14 nm) and FlaA forms a" seam‐like" sheath around the core. The mutant without the sheath has thin PFs (14 nm). By contrast, the wild type has thick PFs (21 nm). This report demonstrates a unique role of multiple flagellin proteins in spirochete flagellation and motility by using an approach of genetics, biochemistry, and cryo‐electron tomography and provides new insights into understanding the complexity and structure of flagellar filament, a helical propeller for bacterial locomotion.