Characterization of a novel Spirillum-like bacterium that degrades ferrioxamine-type siderophores

Abstract

A novel Gram-negative Spirillum-like bacterium (ASP-1) was isolated from lake water by enrichment culture on desferrioxamine B as sole source of carbon and energy. ASP-1 was able to degrade the siderophores desferrioxamine B and E. The property of siderophore degradation was inducible in the presence of desferrioxamine B. The ferric complexes, however, were not measurably degraded but served as an iron source. Degradation of desferrioxamines in culture was followed by measuring the residual ferrioxamines colorimetrically at 430 nm after addition of iron. Degradation in cell-free assays was followed quantitatively by HPLC on a reversed-phase column measuring the time-dependent disappearance of the desferrioxamines B and E. Cell-free assays also revealed that degradation of the cyclic desferrioxamine E was rapid and complete, whereas degradation of the linear desferrioxamine B yielded two intermediate iron-binding metabolites of shorter chain length. Preparative isolation by HPLC and mass spectrometric analysis of the metabolites revealed masses at 361 and 419 a.m.u., respectively, suggesting a splitting at the two amide bonds. ASP-1 is a nitrogen fixing Spirillum bacterium which could also use ammonium and glucose or several organic acids as a carbon source but grew poorly with amino acids. Physiological comparisons with Aquaspirillum and Azospirillum failed to assign ASP-1 to any of the presently known Spirillum species. Based on 16S rDNA sequence analysis the strain could be placed within the radiation of the Azospirillum/Rhodocista group. The closest relative was Azospirillum irakense, showing 98.8% similarity.

Resuscitation by Ferrioxamine E of Stressed Salmonella enterica Serovar Typhimurium from Soil and Water Microcosms

“…Moreover, microcosms of Escherichia coli strains, which do not utilize ferioxamines as sources of iron (6), also do not show extended culturability upon incubation with ferrioxamine E (data not shown). It is unlikely that these effects are due to ferrioxamine E degradation as a source of utilizable carbon, as was recently reported for desferrioxamine B with a Spirillum spp.-like bacterium (15), since Salmonella strains did not grow in minimal media in which the only organic component was ferrioxamine (unpublished data). Rather, we propose that the phenomenon depends upon the fact that ferrioxamine E (an iron-saturated complex with 1:1 stoichiometry) not only supplies iron to bacteria that may have been severely iron starved for prolonged periods but also, by balancing release (e.g., by reduction) and use (in respiration, growth, etc.)…”

Degradation Pathway and Generation of Monohydroxamic Acids from the Trihydroxamate Siderophore Deferrioxamine B

“…M. loti's ability to mineralize DFB, a siderophore produced by the soil microbe Streptomyces pilosus and other soil Streptomyces spp. (10,31,32,36,37), is another such example.…”

“…Three siderophore-degrading microbes, a pseudomonad (33)(34)(35), Azospirillum irakense (36,37), and Mesorhizobium loti (4,7,17,39), catabolize siderophores concomitant with their growth. Neilands and colleagues (33)(34)(35) observed that their microbe, named Pseudomonas FC1, degraded the hydroxamate siderophores ferrichrome, ferrichrome A, and coprogen, with ferrichrome A being the most facile to degrade.…”

“…irakense, isolated from lake water, is a nitrogen fixer and degrades the trihydroxamic acid siderophores deferrioxamines B (DFB) and E (36,37). Similar to that of Pseudomonas FC1, the bacterium's ability to degrade siderophores is inducible, and the enzyme(s) responsible for initiation of siderophore degradation is cellular.…”

Ecology of siderophores with special reference to the fungi

“…The better iron donation properties of mono-and dihydroxamates compared to trishydroxamates may correlate well with the role of plant (leaf)plasma membranebound ferric-chelate reductase (Brü ggemann et al 1993) which reduces ferric citrate and Fe-EDTA in a NADH-dependent mode. Although in general siderophores seem to be very resistant in soil, bacteria of the genus Azospirillum are able to degrade ferrioxamines when present as iron-free compounds (desferrioxmines) in pure culture (Winkelmann et al 1996(Winkelmann et al , 1999. This is surprising as accumulation of desferrioxamines in soil is unlikely.…”