Research Article: Bacterial Flagella: Twist and Stick, or Dodge across the Kingdoms

Date Published: January 15, 2015

Publisher: Public Library of Science

Author(s): Yannick Rossez, Eliza B. Wolfson, Ashleigh Holmes, David L. Gally, Nicola J. Holden, James B. Bliska.

http://doi.org/10.1371/journal.ppat.1004483

Abstract

The flagellum organelle is an intricate multiprotein assembly best known for its rotational propulsion of bacteria. However, recent studies have expanded our knowledge of other functions in pathogenic contexts, particularly adherence and immune modulation, e.g., for Salmonella enterica, Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli. Flagella-mediated adherence is important in host colonisation for several plant and animal pathogens, but the specific interactions that promote flagella binding to such diverse host tissues has remained elusive. Recent work has shown that the organelles act like probes that find favourable surface topologies to initiate binding. An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components. At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms. Bacteria have evolved different strategies to evade or even promote this specific recognition, with some important differences shown for phytopathogens. These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

Partial Text

The prokaryotic flagellum is best known as a motility organelle responsible for bacterial movement and necessary for chemotaxis [1]. An extraordinary multisubunit organelle, complex in its regulation and assembly, the flagellum has been the subject of extensive research over the past four decades and a central topic of evolutionary debate [2]. Ongoing research is still revealing surprises in various aspects, from assembly to function [3,4].

A role for flagella-mediated adherence has been demonstrated in many different plant species and animal infection models, for both pathogenic and opportunistic bacteria [4,5]. These results reveal a significant role for flagella during colonisation and, consequently, environmental transmission. Other factors also facilitate adherence, including electrostatic charge, or specific fimbrial-mediated interactions that may occur at subsequent stages and confer tissue tropism.

Flagellar-mediated host interactions incur a cost, as conserved regions in flagellin monomers are potent inducers of innate immune responses in vivo, across kingdoms. Consequently, recognition of flagellin leads to the greater clearance of flagellated versus nonflagellated strains [20,53–55]. Therefore, there are many immunomodulatory strategies, the simplest being alteration of flagella production and selection of bacteria that are less flagellate upon host-cell contact [56].

Flagella enable pathogens to exploit or capitalise on various niches associated with the host. Although they display a range of functions, these are intrinsically linked to host colonisation and their own biophysical properties. Flagella are therefore not a virulence factor per se, but rather an early stage colonisation factor. They facilitate individual, pioneering cells to access, bind and invade new plant and animal tissues, and if successful in avoiding host recognition and clearance, to establish new colonies. More work is needed to understand how bacteria progress from flagella expression to flagella disassembly, both in the context of expression of more specialised colonisation factors that target specific ligands, and in immune recognition. The location of known ligands and the differences between decoys and membrane bound receptors also need to be addressed. Undoubtedly, future research will uncover further surprises for “twist and stick” or “dodge” flagella.

 

Source:

http://doi.org/10.1371/journal.ppat.1004483