Adaptor-mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation

The Lon AAA+ protease is a highly conserved intracellular protease that is considered an anticancer target in eukaryotic cells and a crucial virulence regulator in bacteria. Lon degrades both damaged, misfolded proteins and specific native regulators, but how Lon discriminates among a large pool of candidate targets remains unclear. Here we report that Bacillus subtilis LonA specifically degrades the master regulator of flagellar biosynthesis SwrA governed by the adaptor protein swarming motility inhibitor A (SmiA). SmiA-dependent LonA proteolysis is abrogated upon microbe-substrate contact causing SwrA protein levels to increase and elevate flagellar density above a critical threshold for swarming motility atop solid surfaces. Surface contact-dependent cellular differentiation in bacteria is rapid, and regulated proteolysis may be a general mechanism of transducing surface stimuli. Significance Bacteria are thought to change physiology when in contact with a solid surface, but the mechanism of surface-contact signal transduction and the output physiological changes are often poorly understood. Here, we show that Bacillus subtilis controls flagellar density by regulatory proteolysis of the master flagellar activator protein SwrA. We further show that the broadly conserved AAA+ protease LonA degrades SwrA only in the presence of swarming motility inhibitor A, the first substrate-specific adaptor protein reported for the Lon family. We propose that surface contact inhibits proteolytic turnover such that SwrA accumulates and the cells synthesize flagella in excess of a critical threshold required for swarming migration.