The two TonB systems of Vibrio cholerae: redundant and specific functions

Abstract

SummaryThe two TonB systems in Vibrio cholerae were found to have unique as well as common functions. Both systems can mediate transport of haemin and the siderophores vibriobactin and ferrichrome. However, TonB1 specifically mediates utilization of the siderophore schizokinen, whereas TonB2 is required for utilization of enterobactin by V. cholerae. Although either TonB system was sufficient for the use of haemin as an iron source, in vitro competition between TonB1 and TonB2 system mutants indicates a preferential role for TonB1 in haemin utilization. This was most pronounced in conditions of high osmolarity, in which TonB1 system mutants were unable to grow with haemin as the sole iron source. Sequence analysis predicted that the two TonB proteins differ in both amino acid sequence and protein size. An internal deletion in TonB1 was constructed in order to generate a protein of approximately the same size as TonB2. A strain expressing the TonB1 deletion protein, and no other TonB, used haemin as the iron source in low-osmolarity medium, but could not use haemin in high osmolarity. This is the same phenotype as a strain expressing only TonB2 and suggests that TonB1, but not TonB2, can span the increased periplasmic space in high osmolarity and thus mediate haemin transport. Mouse colonization assays indicated a role for both TonB systems, and mutations in either system resulted in reduced ability to compete with the wild type in vivo.

Colicin Biology

“…For example, in vitro, a significant interaction between TonB and FhuA can occur in the absence of the ligand ferric ferricrocin (335), but in vivo, TonB apparently cannot transduce energy to nonliganded OM transporters (380). In addition, as noted above, the proline-rich domain can be deleted without inactivating TonB in vivo (382,580), but in vitro, it is required for the formation of the 2:1 complex with FhuA believed to represent TonB at the OM (336).…”

A mutant in one of two exbD loci of a TonB system in Flavobacterium psychrophilum shows attenuated virulence and confers protection against cold water disease

“…In pathogenic bacteria, these ironacquisition systems allow the bacteria to scavenge iron and grow inside the host. Therefore, the TonB system is associated with mechanisms involved in the progress of infection in several important pathogens such as Vibrio cholerae (Seliger et al, 2001), Shigella dysenteriae (Reeves et al, 2000;Payne et al, 2006), uropathogenic Escherichia coli (Torres et al, 2001) and Bordetella pertussis (Pradel et al, 2000). In the bacteria fish pathogens Yersinia ruckeri (Fernández et al, 2004) and Vibrio anguillarum (Stork et al, 2004) a relationship between genes related to TonB systems and virulence has been reported.…”

Vibrio Iron Transport: Evolutionary Adaptation to Life in Multiple Environments

“…Interestingly, the vibrios have more than one set of TonB/ Exb proteins. V. cholerae (33,120,135), V. anguillarum (136), and V. alginolyticus (116) have two TonB systems, and V. vulnificus (137) has three. These systems differ in their recognition of specific receptors and in the environments in which they function, as discussed below.…”

“…Analysis of the TonB1 and TonB2 systems indicates that they have overlapping functions but are not fully redundant. Vibriobactin and ferrichrome are transported efficiently using either TonB1 or TonB2 (33,135). Either TonB system also allowed heme transport via HutA and HutR, although transport was more efficient in strains carrying the tonB1 system genes (120).…”

“…TonB1 interacts with a restricted group of V. cholerae receptors but has the ability to function under environmental conditions, i.e., growth with high salt levels, that do not allow TonB2 to support transport through some receptors (135). TonB1 is 38 amino acids longer than TonB2, and most of this extension maps to the proline-rich region that spans the periplasm.…”