Regulation of mycolactone, the Mycobacterium ulcerans toxin, depends on nutrient source

PLoS Negl Trop Dis. 2013 Nov 14;7(11):e2502. doi: 10.1371/journal.pntd.0002502. eCollection 2013 Nov.

Abstract

Background: Mycobacterium ulcerans, a slow-growing environmental bacterium, is the etiologic agent of Buruli ulcer, a necrotic skin disease. Skin lesions are caused by mycolactone, the main virulence factor of M. ulcerans, with dermonecrotic (destruction of the skin and soft tissues) and immunosuppressive activities. This toxin is secreted in vesicles that enhance its biological activities. Nowadays, it is well established that the main reservoir of the bacilli is localized in the aquatic environment where the bacillus may be able to colonize different niches. Here we report that plant polysaccharides stimulate M. ulcerans growth and are implicated in toxin synthesis regulation.

Methodology/principal findings: In this study, by selecting various algal components, we have identified plant-specific carbohydrates, particularly glucose polymers, capable of stimulating M. ulcerans growth in vitro. Furthermore, we underscored for the first time culture conditions under which the polyketide toxin mycolactone, the sole virulence factor of M. ulcerans identified to date, is down-regulated. Using a quantitative proteomic approach and analyzing transcript levels by RT-qPCR, we demonstrated that its regulation is not at the transcriptional or translational levels but must involve another type of regulation. M. ulcerans produces membrane vesicles, as other mycobacterial species, in which are the mycolactone is concentrated. By transmission electron microscopy, we observed that the production of vesicles is independent from the toxin production. Concomitant with this observed decrease in mycolactone production, the production of mycobacterial siderophores known as mycobactins was enhanced.

Conclusions/significance: This work is the first step in the identification of the mechanisms involved in mycolactone regulation and paves the way for the discovery of putative new drug targets in the future.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Macrolides / metabolism*
  • Mycobacterium ulcerans / metabolism*
  • Proteomics
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • Macrolides
  • mycolactone

Grants and funding

This study was supported by the Fondation Raoul Follereau (http://www.raoul-follereau.org/), the Institut National de la Santé et de la Recherche Médicale (Inserm, Programme Inserm Avenir)(http://www.inserm.fr/); Agence Nationale de la Recherche (ANR 11 CEPL 007 (EXTRA-MU))(http://www.agence-nationale-recherche.fr/), institutional grants from the University of Angers (http://www.univ-angers.fr/), Région Pays de la Loire (ARMINA project)(http://www.paysdelaloire.fr/). CD is funded by post-doctoral grants from Conseil Général Maine-et-Loire (http://www.cg49.fr/) and Angers Loire Métropole (http://www.angersloiremetropole.fr/) and Axa Research Fund (http://www.axa-research.org/) and ANR 11 CEPL 007 (EXTRA-MU). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.