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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

Proposed mechanism of iron mobilization from nontronite. Under iron deficient conditions, P. aeruginosa produces pyoverdine that chelates and solubilizes Fe(III) from edge sites of octahedral (O) or tetrahedral (T) sheets. The higher occurrence of tetrahedral Fe(III) sites in NAu-2 facilitates iron mobilization compared to NAu-1. Iron from pyoverdine-Fe3+ complexes can be taken up into the bacterial cell to sustain growth. When in direct contact with the mineral particles, P. aeruginosa can acquire iron via a siderophore-independent mechanism.
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Figure 7: Proposed mechanism of iron mobilization from nontronite. Under iron deficient conditions, P. aeruginosa produces pyoverdine that chelates and solubilizes Fe(III) from edge sites of octahedral (O) or tetrahedral (T) sheets. The higher occurrence of tetrahedral Fe(III) sites in NAu-2 facilitates iron mobilization compared to NAu-1. Iron from pyoverdine-Fe3+ complexes can be taken up into the bacterial cell to sustain growth. When in direct contact with the mineral particles, P. aeruginosa can acquire iron via a siderophore-independent mechanism.

Mentions: To test whether a direct contact would alleviate the need for pyoverdine, a bfrB-gfp gene fusion constructed in pPROBE-NT was introduced into P. aeruginosa PAO1 ΔpvdD ΔpchEF, The expression of the bfrB gene encoding a bacterioferritin involved in iron storage is induced under iron-replete conditions and, therefore, high expression levels of this gene would indicate that the cells satisfied their metabolic Fe requirement (Parrello et al., 2015). P. aeruginosa ΔpvdD ΔpchEF/pPROBE-bfrB was incubated in direct contact with NAu-1 and NAu-2. The induction of bfrB gene expression was estimated by measuring the GFP fluorescence after 24 h of incubation (Figure 6). The images of bacterial cell aggregates show an expression of bfrB gene in the presence of nontronite, with a higher expression level when the experiment was run with NAu-2 (Figure 6B) compared to NAu-1. This reinforced our previous observations (Figures 1, 4) that the bioavailability of Fe is controlled by the crystallography of the mineral. Furthermore, the siderophore-deficient mutant was able to acquire Fe, which was not readily available for biological uptake, when a physical contact was established with the mineral. A simplified scheme for Fe release from iron bearing clays such as nontronites is proposed in Figure 7.


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

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

Proposed mechanism of iron mobilization from nontronite. Under iron deficient conditions, P. aeruginosa produces pyoverdine that chelates and solubilizes Fe(III) from edge sites of octahedral (O) or tetrahedral (T) sheets. The higher occurrence of tetrahedral Fe(III) sites in NAu-2 facilitates iron mobilization compared to NAu-1. Iron from pyoverdine-Fe3+ complexes can be taken up into the bacterial cell to sustain growth. When in direct contact with the mineral particles, P. aeruginosa can acquire iron via a siderophore-independent mechanism.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814481&req=5

Figure 7: Proposed mechanism of iron mobilization from nontronite. Under iron deficient conditions, P. aeruginosa produces pyoverdine that chelates and solubilizes Fe(III) from edge sites of octahedral (O) or tetrahedral (T) sheets. The higher occurrence of tetrahedral Fe(III) sites in NAu-2 facilitates iron mobilization compared to NAu-1. Iron from pyoverdine-Fe3+ complexes can be taken up into the bacterial cell to sustain growth. When in direct contact with the mineral particles, P. aeruginosa can acquire iron via a siderophore-independent mechanism.
Mentions: To test whether a direct contact would alleviate the need for pyoverdine, a bfrB-gfp gene fusion constructed in pPROBE-NT was introduced into P. aeruginosa PAO1 ΔpvdD ΔpchEF, The expression of the bfrB gene encoding a bacterioferritin involved in iron storage is induced under iron-replete conditions and, therefore, high expression levels of this gene would indicate that the cells satisfied their metabolic Fe requirement (Parrello et al., 2015). P. aeruginosa ΔpvdD ΔpchEF/pPROBE-bfrB was incubated in direct contact with NAu-1 and NAu-2. The induction of bfrB gene expression was estimated by measuring the GFP fluorescence after 24 h of incubation (Figure 6). The images of bacterial cell aggregates show an expression of bfrB gene in the presence of nontronite, with a higher expression level when the experiment was run with NAu-2 (Figure 6B) compared to NAu-1. This reinforced our previous observations (Figures 1, 4) that the bioavailability of Fe is controlled by the crystallography of the mineral. Furthermore, the siderophore-deficient mutant was able to acquire Fe, which was not readily available for biological uptake, when a physical contact was established with the mineral. A simplified scheme for Fe release from iron bearing clays such as nontronites is proposed in Figure 7.

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