Hunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia

Abstract

Low molecular weight siderophores are used by many living organisms to scavenge scarcely available ferric iron. Presence of at least a single siderophore-based iron acquisition system is usually acknowledged as a virulence-associated trait and a pre-requisite to become an efficient and successful pathogen. Currently, it is assumed that yersiniabactin (Ybt) is the solely functional endogenous siderophore iron uptake system in highly virulent Yersinia (Yersinia pestis, Y. pseudotuberculosis, and Y. enterocolitica biotype 1B). Genes responsible for biosynthesis, transport, and regulation of the yersiniabactin (ybt) production are clustered on a mobile genetic element, the High-Pathogenicity Island (HPI) that is responsible for broad dissemination of the ybt genes in Enterobacteriaceae. However, the ybt gene cluster is absent from nearly half of Y. pseudotuberculosis O3 isolates and epidemic Y. pseudotuberculosis O1 isolates responsible for the Far East Scarlet-like Fever. Several potential siderophore-mediated iron uptake gene clusters are documented in Yersinia genomes, however, neither of them have been proven to be functional. It has been suggested that at least two siderophores alternative to Ybt may operate in the highly virulent Yersinia pestis/Y. pseudotuberculosis group, and are referred to as pseudochelin (Pch) and yersiniachelin (Ych). Furthermore, most sporadic Y. pseudotuberculosis O1 strains possess gene clusters encoding all three iron scavenging systems. Thus, the Ybt system appears not to be the sole endogenous siderophore iron uptake system in the highly virulent yersiniae and may be efficiently substituted and/or supplemented by alternative iron siderophore scavenging systems.

Keywords: epidemic Yersinia; highly virulent Yersinia; iron acquisition; pathogenomics; siderophores.

Figure 1

Yersiniabactin gene cluster in Y. pseudotuberculosis O1 (A) and its truncated form in Y. pseudotuberculosis O3 (B).

Figure 2

Comparison of the ybt and ynp iron acquisition clusters in Y. pseudotuberculosis IP32953.

Figure 3

Comparison of the alc-cluster encoding the production of the alcaligin siderophore in Bordetella spp with the ysu-cluster encoding the production of the yersiniachelin siderophore in Y. pestis. Siderophore biosynthetic genes are shown in blue, transport genes—in orange, regulatory gene—in green, and ferric reductase genes with unknown function—in grey.