A mathematical model of biofilm growth and spread within plant xylem: Case study of Xylella fastidiosa in olive trees

J Theor Biol. 2024 Mar 21:581:111737. doi: 10.1016/j.jtbi.2024.111737. Epub 2024 Jan 25.

Abstract

Xylem-limited bacterial pathogens cause some of the most destructive plant diseases. Though imposed measures to control these pathogens are generally ineffective, even among susceptible taxa, some hosts can limit bacterial loads and symptom expression. Mechanisms by which this resistance is achieved are poorly understood. In particular, it is still unknown how differences in vascular structure may influence biofilm growth and spread within a host. To address this, we developed a novel theoretical framework to describe biofilm behaviour within xylem vessels, adopting a polymer-based modelling approach. We then parameterised the model to investigate the relevance of xylem vessel diameters on Xylella fastidiosa resistance among olive cultivars. The functionality of all vessels was severely reduced under infection, with hydraulic flow reductions of 2-3 orders of magnitude. However, results suggest wider vessels act as biofilm incubators; allowing biofilms to develop over a long time while still transporting them through the vasculature. By contrast, thinner vessels become blocked much earlier, limiting biofilm spread. Using experimental data on vessel diameter distributions, we were able to determine that a mechanism of resistance in the olive cultivar Leccino is a relatively low abundance of the widest vessels, limiting X. fastidiosa spread.

Keywords: Biofilm formation; Multiphase model; Olive; Xylella fastidiosa; Xylem-limited bacterial pathogen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biofilms
  • Models, Theoretical
  • Olea* / metabolism
  • Olea* / microbiology
  • Plant Diseases / microbiology
  • Xylella*
  • Xylem

Supplementary concepts

  • Xylella fastidiosa