The role of L-arabinose metabolism for Escherichia coli O157:H7 in edible plants

Louise Crozier, Jacqueline Marshall, Ashleigh Holmes, Kathryn Wright, Yannick Rossez, Bernhard Merget, Sonia Humphris, Ian Toth, Robert Jackson, Nicola Holden

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Abstract

Arabinose is a major plant aldopentose in the form of arabinans complexed in cell wall polysaccharides or glycoproteins (AGP), but comparatively rare as a monosaccharide. l-arabinose is an important bacterial metabolite, accessed by pectolytic micro-organisms such as Pectobacterium atrosepticum via pectin and hemicellulose degrading enzymes. However, not all plant-associated microbes encode cell-wall-degrading enzymes, yet can metabolize l-arabinose, raising questions about their use of and access to the glycan in plants. Therefore, we examined l-arabinose metabolism in the food-borne pathogen Escherichia coli O157:H7 (isolate Sakai) during its colonization of plants. l-arabinose metabolism (araBA) and transport (araF) genes were activated at 18 °C in vitro by l-arabinose and expressed over prolonged periods in planta. Although deletion of araBAD did not impact the colonization ability of E. coli O157:H7 (Sakai) on spinach and lettuce plants (both associated with STEC outbreaks), araA was induced on exposure to spinach cell-wall polysaccharides. Furthermore, debranched and arabinan oligosaccharides induced ara metabolism gene expression in vitro, and stimulated modest proliferation, while immobilized pectin did not. Thus, E. coli O157:H7 (Sakai) can utilize pectin/AGP-derived l-arabinose as a metabolite. Furthermore, it differs fundamentally in ara gene organization, transport and regulation from the related pectinolytic species P. atrosepticum, reflective of distinct plant-associated lifestyles.
Original languageEnglish
Article number001070
Pages (from-to)1-12
Number of pages12
JournalMicrobiology
Volume167
Issue number7
DOIs
Publication statusPublished - 28 Jul 2021

Bibliographical note

Funding Information:
We are grateful for support of Professor Simon Andrews and Professor Carol Wagstaff (University of Reading) to L.C. during her PhD. The araC knockout mutant was a generous gift from Professor Andrew Roe, University of Glasgow, constructed by Dr James Connolly (currently University of Newcastle).

Funding Information:
N.H., R.W.J., I.T. and L.C. were supported by a PhD studentship funded by the James Hutton Institute and the University of Reading; N.H., J.M., A.H., B.M., S.H. and K.W. were supported by the Scottish Government Strategic funding (RD3.1.3, RD2.3.3); N.H. and Y.R. was supported by a Leverhulme Trust grant (RPG-096).

Publisher Copyright:
© 2021 The Authors.

Keywords

  • bacterial pathogens
  • food safety
  • plant-microbe interactions
  • plant cell wall degrading enzymes
  • vegetables

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