An ATP-dependent partner switch links flagellar C-ring assembly with gene expression
Blagotinsek, VitanCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, 35043 Marburg, Germany - Department of Chemistry, Philipps-University Marburg, 35043 Marburg, Germany
Schwan, MeikeDepartment of Microbiology and Molecular Biology, Justus-Liebig-Universität, 35392 Giessen, Germany
Steinchen, WielandCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, 35043 Marburg, Germany - Department of Chemistry, Philipps-University Marburg, 35043 Marburg, Germany
Mrusek, DevidCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, 35043 Marburg, Germany - Department of Chemistry, Philipps-University Marburg, 35043 Marburg, Germany
Hook, John C.Department of Microbiology and Molecular Biology, Justus-Liebig-Universität, 35392 Giessen, Germany
Rossmann, FlorianDepartment of Microbiology and Molecular Biology, Justus-Liebig-Universität, 35392 Giessen, Germany - Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
Freibert, Sven A.Institut für Zytobiologie und Zytopathologie, Philipps-Universität Marburg, 35032 Marburg, Germany
Kratzat, HannaGenzentrum, Ludwig-Maximilians-Universität, 81377 Munich, Germany - Department of Biochemistry, Ludwig-Maximilians-Universität, 81377 Munich, Germany
Murat, GuillaumeDepartment of Biology, University of Fribourg, 1700 Fribourg, Switzerland
Kressler, DieterDepartment of Biology, University of Fribourg, 1700 Fribourg, Switzerland
Beckmann, RolandGenzentrum, Ludwig-Maximilians-Universität, 81377 Munich, Germany - Department of Biochemistry, Ludwig-Maximilians-Universität, 81377 Munich, Germany
Beeby, MorganDepartment of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
Thormann, Kai M.Department of Microbiology and Molecular Biology, Justus-Liebig-Universität, 35392 Giessen, Germany
Bange, GertCenter for Synthetic Microbiology (SYNMIKRO), Philipps-University Marburg, 35043 Marburg, Germany - Department of Chemistry, Philipps-University Marburg, 35043 Marburg, Germany
Proceedings of the National Academy of Sciences. - 2020, vol. 117, no. 34, p. 20826–20835
English
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.