Escherichia coli O157:H7 F9 Fimbriae Recognize Plant Xyloglucan and Elicit a Response in Arabidopsis thaliana.

Ashleigh Holmes,Yannick Rossez,William George Tycho Willats,Jenny Morris,Pete Edward Hedley,Kathryn Mary Wright,Nicola Jean Holden

doi:10.3390/ijms21249720

Abstract

Fresh produce is often a source of enterohaemorrhagic Escherichia coli (EHEC) outbreaks. Fimbriae are extracellular structures involved in cell-to-cell attachment and surface colonisation. F9 (Fml) fimbriae have been shown to be expressed at temperatures lower than 37 °C, implying a function beyond the mammalian host. We demonstrate that F9 fimbriae recognize plant cell wall hemicellulose, specifically galactosylated side chains of xyloglucan, using glycan arrays. E. coli expressing F9 fimbriae had a positive advantage for adherence to spinach hemicellulose extract and tissues, which have galactosylated oligosaccharides as recognized by LM24 and LM25 antibodies. As fimbriae are multimeric structures with a molecular pattern, we investigated whether F9 fimbriae could induce a transcriptional response in model plant Arabidopsis thaliana, compared with flagella and another fimbrial type, E. coli common pilus (ECP), using DNA microarrays. F9 induced the differential expression of 435 genes, including genes involved in the plant defence response. The expression of F9 at environmentally relevant temperatures and its recognition of plant xyloglucan adds to the suite of adhesins EHEC has available to exploit the plant niche.

Highlights

Enterohaemorrhagic Escherichia coli (EHEC) serotype O157:H7 are responsible for food-borne diseases including haemorrhagic colitis or life-threatening complications, such as haemolytic uremic syndrome (HUS) [1], and are frequently associated with outbreaks linked to fresh produce [2]
Phylogenetic analysis of E. coli identified another chaperone-usher pathway (CUP) gene cluster, F9 fimbriae, as part of the γ1 fimbrial subclade, which formed a monophyletic cluster with type 1 fimbriae, suggesting that they originated through gene duplication from a common ancestral operon [10]
We show that F9 fimbriae invoke a host response in Arabidopsis thaliana that is distinct from the response to either H7 flagella or E. coli common pilus (ECP) fimbriae

Summary

Introduction

Enterohaemorrhagic Escherichia coli (EHEC) serotype O157:H7 are responsible for food-borne diseases including haemorrhagic colitis or life-threatening complications, such as haemolytic uremic syndrome (HUS) [1], and are frequently associated with outbreaks linked to fresh produce [2]. Type 1 and P fimbriae are the best characterized structures and belong to a large family of bacterial adhesins, defined by their secretion mechanism, the chaperone-usher pathway (CUP). Type 1 fimbriae adhesin (FimH) binds to mannosylated receptors (α1-3 mannan) via N-linked glycans [6]. Yad fimbriae from E. coli K-12 and E. coli common pilus (ECP) are expressed at a low temperature and mediate binding to plant cell walls via xylose and arabinans, respectively [8,9]. Phylogenetic analysis of E. coli identified another CUP gene cluster, F9 fimbriae ( known as Fml/Yde), as part of the γ1 fimbrial subclade, which formed a monophyletic cluster with type 1 fimbriae, suggesting that they originated through gene duplication from a common ancestral operon [10]

Methods

Results

Conclusion