Surface sensing and metabolic signals drive feedback regulation of long polar fimbriae in enterohemorrhagic Escherichia coli O157

Abstract

Bacterial colonization requires coordinated regulation of adhesion structures in response to environmental conditions. While metabolic regulation of adhesin expression is well established, how surface sensing contributes to this regulation remains less understood. Here, we investigated the regulation and function of long polar fimbriae (Lpf) in enterohemorrhagic Escherichia coli O157. We show that the lpf1 and lpf2 promoters integrate metabolic and surface-associated signals through distinct regulatory regions. Bile induces both promoters independently of distal regulatory sequences, whereas these regions repress basal transcription and are required for induction following surface association. Surface-dependent activation of both lpf promoters is reduced in mutants lacking the major fimbrial subunits LpfA1 and LpfA2, but is unaffected by deletion of the distal tip adhesins. Lpf structures also promote surface-dependent activation of ler, a positive regulator of lpf expression, supporting a regulatory feedback circuit linking surface sensing to lpf transcription. Loss of the major fimbrial subunits also impairs colonization in zebrafish, whereas deletion of the tip adhesins does not under the conditions tested. Together, these findings show that Lpf integrate environmental signals through surface-dependent regulatory feedback and identify an additional role for the fimbrial structure during colonization that does not require the tip adhesins.