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Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry.

Parrello D, Zegeye A, Mustin C, Billard P - Front Microbiol (2016)

Bottom Line: Both nontronites released Fe in a particle concentration-dependent manner when incubated with the wild-type P. aeruginosa strain, however iron released from NAu-2 was substantially greater than from NAu-1.The structural Fe present on the edges of NAu-2 rather than NAu-1 particles appears to be more bio-accessible, indicating that the distribution of Fe, in the tetrahedron and/or in the octahedron sites, governs the solubilisation process.Furthermore, we also revealed that P. aeruginosa could acquire iron when in direct contact with mineral particles in a siderophore-independent manner.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Interdisciplinaire des Environnements Continentaux, UMR 7360 Centre National de la Recherche Scientifique - Université de LorraineVandœuvre-lès-Nancy, France; Civil and Environmental Engineering, University of MissouriColumbia, MO, USA.

ABSTRACT
Bacteria living in oxic environments experience iron deficiency due to limited solubility and slow dissolution kinetics of iron-bearing minerals. To cope with iron deprivation, aerobic bacteria have evolved various strategies, including release of siderophores or other organic acids that scavenge external Fe(III) and deliver it to the cells. This research investigated the role of siderophores produced by Pseudomonas aeruginosa in the acquisition of Fe(III) from two iron-bearing colloidal nontronites (NAu-1 and NAu-2), comparing differences in bioavailability related with site occupancy and distribution of Fe(III) in the two lattices. To avoid both the direct contact of the mineral colloids with the bacterial cells and the uncontrolled particle aggregation, nontronite suspensions were homogenously dispersed in a porous silica gel before the dissolution experiments. A multiparametric approach coupling UV-vis spectroscopy and spectral decomposition algorithm was implemented to monitor simultaneously the solubilisation of Fe and the production of pyoverdine in microplate-based batch experiments. Both nontronites released Fe in a particle concentration-dependent manner when incubated with the wild-type P. aeruginosa strain, however iron released from NAu-2 was substantially greater than from NAu-1. The profile of organic acids produced in both cases was similar and may not account for the difference in the iron dissolution efficiency. In contrast, a pyoverdine-deficient mutant was unable to mobilize Fe(III) from either nontronite, whereas iron dissolution occurred in abiotic experiments conducted with purified pyoverdine. Overall, our data provide evidence that P. aeruginosa indirectly mobilize Fe from nontronites primarily through the production of pyoverdine. The structural Fe present on the edges of NAu-2 rather than NAu-1 particles appears to be more bio-accessible, indicating that the distribution of Fe, in the tetrahedron and/or in the octahedron sites, governs the solubilisation process. Furthermore, we also revealed that P. aeruginosa could acquire iron when in direct contact with mineral particles in a siderophore-independent manner.

No MeSH data available.


Related in: MedlinePlus

P. aeruginosa-promoted Fe dissolution from silica gel-embedded nontronites in a system where NAu-1 to NAu-2 ratios are varied across a range of particle concentration, after 24 h of incubation. (A) Fe dissolution for a constant NAu-1 to NAu-2 ratio ([NAu-1]/([NAu-1] + [NAu-2]) = 0) while the particle concentration varied. (B) Fe dissolution for a constant particle concentration (3.3 g L−1) with different NAu-1 to NAu-2 ratios. The symbols represent soluble Fe (squares), KCl extracted Fe (circles), hydroxylamine-KCl extracted Fe (triangles) and the sum of the three above Fe concentrations (stars). Error bars indicate the standard error of the mean (n = 2 for soluble Fe; n = 3 for KCl- and hydroxylamine-KCl extracted Fe).
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Figure 1: P. aeruginosa-promoted Fe dissolution from silica gel-embedded nontronites in a system where NAu-1 to NAu-2 ratios are varied across a range of particle concentration, after 24 h of incubation. (A) Fe dissolution for a constant NAu-1 to NAu-2 ratio ([NAu-1]/([NAu-1] + [NAu-2]) = 0) while the particle concentration varied. (B) Fe dissolution for a constant particle concentration (3.3 g L−1) with different NAu-1 to NAu-2 ratios. The symbols represent soluble Fe (squares), KCl extracted Fe (circles), hydroxylamine-KCl extracted Fe (triangles) and the sum of the three above Fe concentrations (stars). Error bars indicate the standard error of the mean (n = 2 for soluble Fe; n = 3 for KCl- and hydroxylamine-KCl extracted Fe).

Mentions: The multi-way approach consisted of 25 independent assays where the nontronite particle concentrations and NAu-1/NAu-2 ratio were varied all together and incubated with P. aeruginosa for 24 h before spectrophotometric measurement of iron release. For instance, Figure 1A represents the Fe dissolution profile when the assays were run with a constant nontronite ratio (100% of NAu-2 with [NAu-1]/[NAu-1] + [NAu-2] = 0%) across a range of particle concentrations (0 to 3.3 g L−1) in the presence of PAO1 WT. Figure 2A, on the other hand, illustrates the Fe dissolution profile when the assays were run with a constant particle concentration (i.e., 3.3 g L−1) while varying NAu-1 and NAu-2 ratio (i.e., 0 ≤ [NAu-1]/[NAu-1] + [NAu-2] ≤ 100%) in the presence of the same strain. An increase of Fe released in the culture medium was observed with increasing particle concentration indicating that the diffusion of the compounds responsible for the dissolution of Fe, through the porous silica gel was not a limiting factor in the range of tested particle concentrations (Figure 1A). For the assay run with the highest particle concentration (i.e., 3.3 g L−1) a total of 5.18 ± 0.21 μM of Fe were released in the culture media, 58% of which were soluble Fe. The same trend (soluble over total Fe) was noted across the entire particles concentrations tested (Figure 1A). The presence of Fe extracted with KCl and hydroxylamine treatment indicated that a small fraction of iron was adsorbed and/or precipitated on the mineral and/or on the silica gel after dissolution (Figure 1A). Overall the results show that a substantial amount of Fe was liberated in the culture media. Given the fact that NAu particles are highly insoluble at circumneutral pH, the Fe present in the media was likely chelated by organic molecules (i.e., excreted by bacteria), thus becoming available for bacterial uptake. Similarly, the related strain Pseudomonas mendocina ymp requires micromolar concentration of Fe for optimal growth (Dehner et al., 2010). Likewise, the amount of Fe dissolved from NAu-2 in the culture media is sufficient to support P. aeruginosa growth (not shown).


Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry.

Parrello D, Zegeye A, Mustin C, Billard P - Front Microbiol (2016)

P. aeruginosa-promoted Fe dissolution from silica gel-embedded nontronites in a system where NAu-1 to NAu-2 ratios are varied across a range of particle concentration, after 24 h of incubation. (A) Fe dissolution for a constant NAu-1 to NAu-2 ratio ([NAu-1]/([NAu-1] + [NAu-2]) = 0) while the particle concentration varied. (B) Fe dissolution for a constant particle concentration (3.3 g L−1) with different NAu-1 to NAu-2 ratios. The symbols represent soluble Fe (squares), KCl extracted Fe (circles), hydroxylamine-KCl extracted Fe (triangles) and the sum of the three above Fe concentrations (stars). Error bars indicate the standard error of the mean (n = 2 for soluble Fe; n = 3 for KCl- and hydroxylamine-KCl extracted Fe).
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Related In: Results  -  Collection

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Show All Figures
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Figure 1: P. aeruginosa-promoted Fe dissolution from silica gel-embedded nontronites in a system where NAu-1 to NAu-2 ratios are varied across a range of particle concentration, after 24 h of incubation. (A) Fe dissolution for a constant NAu-1 to NAu-2 ratio ([NAu-1]/([NAu-1] + [NAu-2]) = 0) while the particle concentration varied. (B) Fe dissolution for a constant particle concentration (3.3 g L−1) with different NAu-1 to NAu-2 ratios. The symbols represent soluble Fe (squares), KCl extracted Fe (circles), hydroxylamine-KCl extracted Fe (triangles) and the sum of the three above Fe concentrations (stars). Error bars indicate the standard error of the mean (n = 2 for soluble Fe; n = 3 for KCl- and hydroxylamine-KCl extracted Fe).
Mentions: The multi-way approach consisted of 25 independent assays where the nontronite particle concentrations and NAu-1/NAu-2 ratio were varied all together and incubated with P. aeruginosa for 24 h before spectrophotometric measurement of iron release. For instance, Figure 1A represents the Fe dissolution profile when the assays were run with a constant nontronite ratio (100% of NAu-2 with [NAu-1]/[NAu-1] + [NAu-2] = 0%) across a range of particle concentrations (0 to 3.3 g L−1) in the presence of PAO1 WT. Figure 2A, on the other hand, illustrates the Fe dissolution profile when the assays were run with a constant particle concentration (i.e., 3.3 g L−1) while varying NAu-1 and NAu-2 ratio (i.e., 0 ≤ [NAu-1]/[NAu-1] + [NAu-2] ≤ 100%) in the presence of the same strain. An increase of Fe released in the culture medium was observed with increasing particle concentration indicating that the diffusion of the compounds responsible for the dissolution of Fe, through the porous silica gel was not a limiting factor in the range of tested particle concentrations (Figure 1A). For the assay run with the highest particle concentration (i.e., 3.3 g L−1) a total of 5.18 ± 0.21 μM of Fe were released in the culture media, 58% of which were soluble Fe. The same trend (soluble over total Fe) was noted across the entire particles concentrations tested (Figure 1A). The presence of Fe extracted with KCl and hydroxylamine treatment indicated that a small fraction of iron was adsorbed and/or precipitated on the mineral and/or on the silica gel after dissolution (Figure 1A). Overall the results show that a substantial amount of Fe was liberated in the culture media. Given the fact that NAu particles are highly insoluble at circumneutral pH, the Fe present in the media was likely chelated by organic molecules (i.e., excreted by bacteria), thus becoming available for bacterial uptake. Similarly, the related strain Pseudomonas mendocina ymp requires micromolar concentration of Fe for optimal growth (Dehner et al., 2010). Likewise, the amount of Fe dissolved from NAu-2 in the culture media is sufficient to support P. aeruginosa growth (not shown).

Bottom Line: Both nontronites released Fe in a particle concentration-dependent manner when incubated with the wild-type P. aeruginosa strain, however iron released from NAu-2 was substantially greater than from NAu-1.The structural Fe present on the edges of NAu-2 rather than NAu-1 particles appears to be more bio-accessible, indicating that the distribution of Fe, in the tetrahedron and/or in the octahedron sites, governs the solubilisation process.Furthermore, we also revealed that P. aeruginosa could acquire iron when in direct contact with mineral particles in a siderophore-independent manner.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Interdisciplinaire des Environnements Continentaux, UMR 7360 Centre National de la Recherche Scientifique - Université de LorraineVandœuvre-lès-Nancy, France; Civil and Environmental Engineering, University of MissouriColumbia, MO, USA.

ABSTRACT
Bacteria living in oxic environments experience iron deficiency due to limited solubility and slow dissolution kinetics of iron-bearing minerals. To cope with iron deprivation, aerobic bacteria have evolved various strategies, including release of siderophores or other organic acids that scavenge external Fe(III) and deliver it to the cells. This research investigated the role of siderophores produced by Pseudomonas aeruginosa in the acquisition of Fe(III) from two iron-bearing colloidal nontronites (NAu-1 and NAu-2), comparing differences in bioavailability related with site occupancy and distribution of Fe(III) in the two lattices. To avoid both the direct contact of the mineral colloids with the bacterial cells and the uncontrolled particle aggregation, nontronite suspensions were homogenously dispersed in a porous silica gel before the dissolution experiments. A multiparametric approach coupling UV-vis spectroscopy and spectral decomposition algorithm was implemented to monitor simultaneously the solubilisation of Fe and the production of pyoverdine in microplate-based batch experiments. Both nontronites released Fe in a particle concentration-dependent manner when incubated with the wild-type P. aeruginosa strain, however iron released from NAu-2 was substantially greater than from NAu-1. The profile of organic acids produced in both cases was similar and may not account for the difference in the iron dissolution efficiency. In contrast, a pyoverdine-deficient mutant was unable to mobilize Fe(III) from either nontronite, whereas iron dissolution occurred in abiotic experiments conducted with purified pyoverdine. Overall, our data provide evidence that P. aeruginosa indirectly mobilize Fe from nontronites primarily through the production of pyoverdine. The structural Fe present on the edges of NAu-2 rather than NAu-1 particles appears to be more bio-accessible, indicating that the distribution of Fe, in the tetrahedron and/or in the octahedron sites, governs the solubilisation process. Furthermore, we also revealed that P. aeruginosa could acquire iron when in direct contact with mineral particles in a siderophore-independent manner.

No MeSH data available.


Related in: MedlinePlus