Iron transport in Streptomyces pilosus mediated by ferrichrome siderophores, rhodotorulic acid, and enantio-rhodotorulic acid

Abstract

Streptomyces pilosus is one of several microbes which produce ferrioxamine siderophores. In the accompanying paper (G. Muller and K. Raymond, J. Bacteriol. 160:304-312), the mechanism of iron uptake mediated by the endogenous ferrioxamines B, DI, D2, and E was examined. Here we report iron transport behavior in S. pilosus as mediated by the exogenous siderophores ferrichrome, ferrichrysin, rhodotorulic acid (RA), and synthetic enantio-RA. In each case iron acquisition depended on metabolic energy and had uptake rates comparable to that of [55Fe]ferrioxamine B. However, the synthetic ferric enantio-RA (which has the same preferred chirality at the metal center as fet-richrome) was twice as effective in supplying iron as was the natural ferric RA complex, suggesting that stereospecific recognition at the metal center is involved in the transport process. Iron uptake mediated by ferrichrome and ferric enantio-RA was strongly inhibited by kinetically inert chromic complexes of desferrioxamine B. These inhibition experiments indicate that iron from these exogenous siderophores Is transported by the same uptake system as ferrioxamine B. Since the ligands have no structural similarity to ferrioxamine B except for the presence of three hydoxamate groups, we conclude that only the hydroxamate iron center and its direct surroundings are important for recognition and uptake. This hypothesis is supported by the fact that ferrichrome A and ferrirubin, which are both substituted at the hydroxamate carbonyl groups, were not (or were poorly) effective in supplying iron to S. pilosus.

Differential Siderophore Utilization and Iron Uptake by Soil and Rhizosphere Bacteria

“…Similarly, pseudobactin St3 mediated uptake of 55Fe3' by P. putida St3 much more efficiently than FOB and FC. Uptake rates of 55Fe3+ mediated by FOB and FC were in a range similar to that reported for S. pilosus and E. coli, respectively (25,37).…”

Growth of desferrioxamine-deficientStreptomycesmutants through xenosiderophore piracy of airborne fungal contaminations

“…This hypothesis is supported by previous studies that suggest possible fungal siderophore piracy by streptomycetes, as the exogenous supply of pure ferrichrome, as well as pure coprogen, could partially restore the growth of otherwise uncultivable desferrioxamine (DFO)-null mutants of Streptomyces coelicolor grown in an iron-limited medium (Barona-Gomez et al 2006). Prior to this, Müller, Matzanke and Raymond (1984) had monitored high-affinity xenosiderophore transport by S. pilosus. However, whether fungal siderophore utilization by Streptomyces really occurs in coculture and/or in a natural environment is yet to be shown.…”

“…Combined HPLC fractionation and UPLC-ESI-MS analyses revealed that the 'resuscitation' factors were all siderophores of our Penicillium isolate (Charlang et al 1981;Hordt, Romheld and Winkelmann 2000), demonstrating that S. coelicolor can utilize fungal siderophores in cocultures. Previous in vitro studies have shown the ability of S. coelicolor and S. pilosus to take up pure hydroxamate-containing fungal siderophores (Müller, Matzanke and Raymond 1984;Barona-Gomez et al 2006). DesE, the iron-siderophore binding lipoprotein adjacent to the DFO biosynthetic cluster, and to a lesser extent genes of the tri-cistronic operon cdtCBA encoding a putative ABC transporter for ferric siderophores, have been indicated as xenosiderophore uptake systems in the Streptomyces species (Bunet et al 2006;Patel, Song and Challis 2010).…”

Diverging roles of bacterial siderophores during infection

“…6,[23][24][25] The hydroxamate family of siderophores includes the fungal siderophores ferrichrome and (des)ferrioxamine (DFO; K d = 10 À30 M), a Streptomyces-derived siderophore used clinically to chelate iron. [26][27][28][29][30] Hydroxamate siderophores also form fivemembered chelate rings but have lower affinities for iron than catecholate siderophores. 31 Carboxylate siderophores include staphyloferrin and citrate.…”