Loss of FlhE in the flagellar Type III secretion system allows proton influx into Salmonella and Escherichia coli

Mol Microbiol. 2012 May;84(3):550-65. doi: 10.1111/j.1365-2958.2012.08043.x. Epub 2012 Apr 4.

Abstract

flhE belongs to the flhBAE flagellar operon in Enterobacteria, whose first two members function in Type III secretion (T3S). In Salmonella enterica, absence of FlhE affects swarming, but not swimming, motility. Based on a chance observation of a 'green' colony phenotype of flhE mutants on pH indicator plates containing glucose, we have established that this phenotype is associated with lysis of flagellated cells in an acidic environment created by glucose metabolism. The flhE mutant phenotype of Escherichia coli is similar overall to that of S. enterica but is seen in the absence of glucose and, unlike in S. enterica, causes a substantial growth defect. flhE mutants have a lowered cytoplasmic pH in both bacteria, indicative of a proton leak. GFP reporter assays indicate that the leak is dependent on the flagellar system, is present before the T3S system switches to secretion of late substrates, and gets worse after the switch and upon filament assembly, leading to cell lysis. We show that FlhE is a periplasmic protein that co-purifies with flagellar basal bodies. FlhE may act as a plug or a chaperone to regulate proton flow through the flagellar T3S system.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Bacterial Secretion Systems*
  • Biological Transport
  • Escherichia coli / chemistry
  • Escherichia coli / genetics
  • Escherichia coli / metabolism*
  • Flagella / chemistry
  • Flagella / genetics
  • Flagella / metabolism*
  • Gene Expression Regulation, Bacterial
  • Hydrogen-Ion Concentration
  • Protons
  • Salmonella typhimurium / chemistry
  • Salmonella typhimurium / genetics
  • Salmonella typhimurium / metabolism*
  • Sequence Deletion

Substances

  • Bacterial Proteins
  • Bacterial Secretion Systems
  • Protons