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Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved July 9, 2020 (received for review April 6, 2020)
Significance
Flagella, bacterial organelles of locomotion, appear in a defined number and localization at the bacterial cell surface. The MinD-type ATPase FlhG numerically regulates flagellation patterns through a molecular mechanism only poorly understood. Depending on its ATP-dependent oligomerization state, FlhG interacts either with the C-ring protein FliM during flagellar assembly or with flagellar master regulator FlrA. This partner switch between FliM and FlrA establishes a regulatory network critical for the numerical regulation of flagella, in which the physical assembly of the flagellum transcriptionally feeds back to prevent the production of more building blocks.
Abstract
Bacterial flagella differ in their number and spatial arrangement. In many species, the MinD-type ATPase FlhG (also YlxH/FleN) is central to the numerical control of bacterial flagella, and its deletion in polarly flagellated bacteria typically leads to hyperflagellation. The molecular mechanism underlying this numerical control, however, remains enigmatic. Using the model species Shewanella putrefaciens, we show that FlhG links assembly of the flagellar C ring with the action of the master transcriptional regulator FlrA (named FleQ in other species). While FlrA and the flagellar C-ring protein FliM have an overlapping binding site on FlhG, their binding depends on the ATP-dependent dimerization state of FlhG. FliM interacts with FlhG independent of nucleotide binding, while FlrA exclusively interacts with the ATP-dependent FlhG dimer and stimulates FlhG ATPase activity. Our in vivo analysis of FlhG partner switching between FliM and FlrA reveals its mechanism in the numerical restriction of flagella, in which the transcriptional activity of FlrA is down-regulated through a negative feedback loop. Our study demonstrates another level of regulatory complexity underlying the spationumerical regulation of flagellar biogenesis and implies that flagellar assembly transcriptionally regulates the production of more initial building blocks.
Footnotes
↵1V.B. and M.S. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: Kai.Thormann{at}mikro.bio.uni-giessen.de or gert.bange{at}synmikro.uni-marburg.de.
Author contributions: D.K., K.M.T., and G.B. designed research; V.B., M.S., W.S., D.M., J.C.H., F.R., S.A.F., H.K., and G.M. performed research; R.B. contributed new reagents/analytic tools; V.B., M.S., W.S., D.M., F.R., S.A.F., M.B., K.M.T., and G.B. analyzed data; and M.B., K.M.T., and G.B. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2006470117/-/DCSupplemental.
Data Availability.
All data supporting the findings of this study are included in this paper and SI Appendix.
Published under the PNAS license.
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An ATP-dependent partner switch links flagellar C-ring assembly with gene expression
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