Cargando…

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

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 ex...

Descripción completa

Detalles Bibliográficos
Autores principales: Parrello, Damien, Zegeye, Asfaw, Mustin, Christian, Billard, Patrick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4814481/
https://www.ncbi.nlm.nih.gov/pubmed/27064911
http://dx.doi.org/10.3389/fmicb.2016.00423
_version_ 1782424418510700544
author Parrello, Damien
Zegeye, Asfaw
Mustin, Christian
Billard, Patrick
author_facet Parrello, Damien
Zegeye, Asfaw
Mustin, Christian
Billard, Patrick
author_sort Parrello, Damien
collection PubMed
description 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.
format Online
Article
Text
id pubmed-4814481
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-48144812016-04-08 Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry Parrello, Damien Zegeye, Asfaw Mustin, Christian Billard, Patrick Front Microbiol Microbiology 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. Frontiers Media S.A. 2016-03-31 /pmc/articles/PMC4814481/ /pubmed/27064911 http://dx.doi.org/10.3389/fmicb.2016.00423 Text en Copyright © 2016 Parrello, Zegeye, Mustin and Billard. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Parrello, Damien
Zegeye, Asfaw
Mustin, Christian
Billard, Patrick
Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title_full Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title_fullStr Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title_full_unstemmed Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title_short Siderophore-Mediated Iron Dissolution from Nontronites Is Controlled by Mineral Cristallochemistry
title_sort siderophore-mediated iron dissolution from nontronites is controlled by mineral cristallochemistry
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4814481/
https://www.ncbi.nlm.nih.gov/pubmed/27064911
http://dx.doi.org/10.3389/fmicb.2016.00423
work_keys_str_mv AT parrellodamien siderophoremediatedirondissolutionfromnontronitesiscontrolledbymineralcristallochemistry
AT zegeyeasfaw siderophoremediatedirondissolutionfromnontronitesiscontrolledbymineralcristallochemistry
AT mustinchristian siderophoremediatedirondissolutionfromnontronitesiscontrolledbymineralcristallochemistry
AT billardpatrick siderophoremediatedirondissolutionfromnontronitesiscontrolledbymineralcristallochemistry