MinD-like ATPase FlhG effects location and number of bacterial flagella during C-ring assembly.
The number and location of flagella, bacterial organelles of locomotion, are species specific and appear in regular patterns that represent one of the earliest taxonomic criteria in microbiology. However, the mechanisms that reproducibly establish these patterns during each round of cell division are poorly understood. FlhG (previously YlxH) is a major determinant for a variety of flagellation patterns. Here, we show that FlhG is a structural homolog of the ATPase MinD, which serves in cell-division site determination. Like MinD, FlhG forms homodimers that are dependent on ATP and lipids. It interacts with a complex of the flagellar C-ring proteins FliM and FliY (also FliN) in the Gram-positive, peritrichous-flagellated Bacillus subtilis and the Gram-negative, polar-flagellated Shewanella putrefaciens. FlhG interacts with FliM/FliY in a nucleotide-independent manner and activates FliM/FliY to assemble with the C-ring protein FliG in vitro. FlhG-driven assembly of the FliM/FliY/FliG complex is strongly enhanced by ATP and lipids. The protein shows a highly dynamic subcellular distribution between cytoplasm and flagellar basal bodies, suggesting that FlhG effects flagellar location and number during assembly of the C-ring. We describe the molecular evolution of a MinD-like ATPase into a flagellation pattern effector and suggest that the underappreciated structural diversity of the C-ring proteins might contribute to the formation of different flagellation patterns.
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Jan S
JS
Schuhmacher
Department of Microbiology and Molecular Biology, Justus-Liebig University, 35392 Giessen, Germany; and.
Florian
F
Rossmann
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Felix
F
Dempwolff
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Carina
C
Knauer
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Florian
F
Altegoer
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Wieland
W
Steinchen
Department of Microbiology and Molecular Biology, Justus-Liebig University, 35392 Giessen, Germany; and.
Anja K
AK
Dörrich
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany; Department of Biology I, Ludwig Maximilian University Munich, 82152 Planegg-Martinsried, Germany.
Andreas
A
Klingl
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Milena
M
Stephan
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany;
Uwe
U
Linne
Department of Microbiology and Molecular Biology, Justus-Liebig University, 35392 Giessen, Germany; and.
Kai M
KM
Thormann
LOEWE Center for Synthetic Microbiology (Synmikro) and Department of Chemistry, Philipps University Marburg, 35043 Marburg, Germany; gert.bange@synmikro.uni-marburg.de.
Gert
G
Bange
D001426:Bacterial Proteins / Q000378:metabolism / Q000502:physiology*; D019281:Dimerization; D005407:Flagella / Q000201:enzymology / Q000502:physiology*
D001426:Bacterial Proteins
Bacillus; C-ring; FlhG; Shewanella; flagellum