The Acyl-Homoserine Lactone Synthase YenI from Yersinia enterocolitica Modulates Virulence Gene Expression in Enterohemorrhagic Escherichia coli O157:H7

Abstract

The human pathogen enterohemorrhagic Escherichia coli (EHEC) O157:H7 colonizes the rectoanal junction (RAJ) in cattle, its natural reservoir. Colonization at the RAJ poses a serious risk for fecal shedding and contamination of the environment. We previously demonstrated that EHEC senses acyl-homoserine lactones (AHLs) produced by the microbiota in the rumen to activate the gad acid resistance genes necessary for survival through the acidic stomachs in cattle and to repress the locus of enterocyte effacement (LEE) genes important for colonization of the RAJ, but unnecessary in the rumen. Devoid of AHLs, the RAJ is the prominent site of colonization of EHEC in cattle. To determine if the presence of AHLs in the RAJ could repress colonization at this site, we engineered EHEC to express the Yersinia enterocolitica AHL synthase gene yenI, which constitutively produces AHLs, to mimic a constant exposure of AHLs in the environment. The yenI ؉ EHEC produces oxo-C6-homoserine lactone (oxo-C6-HSL) and had a significant reduction in LEE expression, effector protein secretion, and attaching and effacing (A/E) lesion formation in vitro compared to the wild type (WT). The yenI ؉ EHEC also activated expression of the gad genes. To assess whether AHL production, which decreases LEE expression, would decrease RAJ colonization by EHEC, cattle were challenged at the RAJ with WT or yenI ؉ EHEC. Although the yenI ؉ EHEC colonized the RAJ with efficiency equal to that of the WT, there was a trend for the cattle to shed the WT strain longer than the yenI ؉ EHEC.

Role of SdiA on Biofilm Formation by Atypical Enteropathogenic Escherichia coli

“…The influence of AHL on SdiA was confirmed by analyzing the mutant strains, which showed no significant difference on biofilm formation. Hughes et al [ 32 ], described possible downregulation of ler transcription by AHLs addition in an EHEC strain and lately Nguyen et al [ 53 ], also verified downregulation in ler , espA and tir transcription in an EHEC acyl homoserine synthase ( yenl + ) strain, which produces endogenous AHLs.…”

Response of Lactobacillus plantarum WCFS1 to the Gram-Negative Pathogen-Associated Quorum Sensing Molecule N-3-Oxododecanoyl Homoserine Lactone

“…Indeed, AHL recognition by higher order species has been previously observed (Smith et al, 2002a,b; Mathesius et al, 2003; Ritchie et al, 2003, 2005, 2007; Bauer and Mathesius, 2004; Chun et al, 2004; Wagner et al, 2007; Jahoor et al, 2008; Teplitski et al, 2011; Kariminik et al, 2017) with the rationale that the effects imparted by AHLs are due to their structural and functional resemblance to hormones and phytohormones (Teplitski et al, 2011). Within the bacterial kingdom, investigators have previously noted cross-species effects of a Yersinia enterocolitica AHL on enterohemorrhagic Escherichia coli O157:H7 (Nguyen et al, 2013) and S. aureus -derived peptides on both Enterococcus spp. (Firth et al, 1994) and Lactobacillus reuteri (Lubkowicz et al, 2018).…”

From ingestion to colonization: the influence of the host environment on regulation of the LEE encoded type III secretion system in enterohaemorrhagic Escherichia coli

“…Enterohaemorrhagic Escherichia coli can also sense hormone-like signals produced by members of the microbiota. SdiA is a LuxR-like transcriptional regulator has the remarkable ability of responding to acyl-homoserine lactones produced by neighboring bacteria but not EHEC ( Hughes et al, 2010 ; Nguyen et al, 2013 ). SdiA represses the LEE in response to these signals but also activates expression of GadX known to inhibit LEE1 expression as EHEC passage through the stomach.…”