Effects of exogenous pyoverdines on Fe availability and their impacts on Mn(II) oxidation by Pseudomonas putida GB-1

TitleEffects of exogenous pyoverdines on Fe availability and their impacts on Mn(II) oxidation by Pseudomonas putida GB-1
Publication TypeJournal Article
Year of Publication2014
AuthorsLee S.W, Parker D.L, Geszvain K, Tebo BM
JournalFrontiers in Microbiology
Date Published2014/06
Type of ArticleArticle
ISBN Number1664-302X
Accession NumberWOS:000338732500001
Keywordsaeruginosa; bacillus; biofilm; biofilm formation; biogenic manganese oxides; Fe availability; ferripyoverdine; fluorescent pseudomonas; hydroxamate siderophores; iron limitation; iron requirement; leptothrix-discophora; marine; mediated iron uptake; MnO2; multicopper oxidase; pyoverdine; pyoverdine receptor; receptor; siderotyping

Pseudomonas putida GB-1 is a Mn(II)-oxidizing bacterium that produces pyoverdine-type siderophores (PVDs), which facilitate the uptake of Fe(III) but also influence MnO2 formation. Recently, a non-ribosomal peptide synthetase mutant that does not synthesize PVD was described. Here we identified a gene encoding the PVDGB-1 (PVD produced by strain GB-1) uptake receptor (PputGB1_4082) of strain GB-1 and confirmed its function by in-frame mutagenesis. Growth and other physiological responses of these two mutants and of wild type were compared during cultivation in the presence of three chemically distinct sets of PVDs (siderotypes n degrees 1, n degrees 2, and n degrees 4) derived from various pseudomonads. Under iron-limiting conditions, Fe(III) complexes of various siderotype n degrees 1 PVDs (including PVDGB-1) allowed growth of wild type and the synthetase mutant, but not the receptor mutant, confirming that iron uptake with any tested siderotype n degrees 1 PVD depended on PputGB1_4082. Fe(III) complexes of a siderotype n degrees 2 PVD were not utilized by any strain and strongly induced PVD synthesis. In contrast, Fe(III) complexes of siderotype n degrees 4 PVDs promoted the growth of all three strains and did not induce PVD synthesis by the wild type, implying these complexes were utilized for iron uptake independent of PputGB1_4082. These differing properties of the three PVD types provided a way to differentiate between effects on MnO2 formation that resulted from iron limitation and others that required participation of the PVDGB-1 receptor. Specifically, MnO2 production was inhibited by siderotype n degrees 1 but not n degrees 4 PVDs indicating PVD synthesis or PputGB1_4082 involvement rather than iron-limitation caused the inhibition. In contrast, iron limitation was sufficient to explain the inhibition of Mn(II) oxidation by siderotype n degrees 2 PVDs. Collectively, our results provide insight into how competition for iron via siderophores influences growth, iron nutrition and MnO2 formation in more complex environmental systems.

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