Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria

Jennyfer Miot; Karim Benzerara; Guillaume Morin; Andreas Kappler; Sylvain Bernard; Martin Obst; Céline Férard; Fériel Skouri-Panet; Jean Michel Guigner; Nicole Posth; Matthieu Galvez; Gordon E. Brown; François Guyot

doi:10.1016/j.gca.2008.10.033

Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria

Jennyfer Miot, Karim Benzerara, Guillaume Morin, Andreas Kappler, Sylvain Bernard, Martin Obst, Céline Férard, Fériel Skouri-Panet, Jean Michel Guigner, Nicole Posth, Matthieu Galvez, Gordon E. Brown, François Guyot

Geology

206 Citations (Scopus)

Abstract

Minerals formed by bio-oxidation of ferrous iron (Fe(II)) at neutral pH, their association with bacterial ultrastructures as well as their impact on the metabolism of iron-oxidizing bacteria remain poorly understood. Here, we investigated iron biomineralization by the anaerobic nitrate-dependent iron-oxidizing bacterium Acidovorax sp. strain BoFeN1 in the presence of dissolved Fe(II) using electron microscopy and Scanning Transmission X-ray Microscopy (STXM). All detected minerals consisted mainly of amorphous iron phosphates, but based on their morphology and localization, three types of precipitates could be discriminated: (1) mineralized filaments at distance from the cells, (2) globules of 100 ± 25 nm in diameter, at the cell surface and (3) a 40-nm thick mineralized layer within the periplasm. All of those phases were shown to be intimately associated with organic molecules. Periplasmic encrustation was accompanied by an accumulation of protein moieties. In the same way, exopolysaccharides were associated with the extracellular mineralized filaments. The evolution of cell encrustation was followed by TEM over the time course of a culture: cell encrustation proceeded progressively, with rapid precipitation in the periplasm (in a few tens of minutes), followed by the formation of surface-bound globules. Moreover, we frequently observed an asymmetric mineral thickening at the cell poles. In parallel, the evolution of iron oxidation was quantified by STXM: iron both contained in the bacteria and in the extracellular precipitates reached complete oxidation within 6 days. While a progressive oxidation of Fe in the bacteria and in the medium could be observed, spatial redox (oxido-reduction state) heterogeneities were detected at the cell poles and in the extracellular precipitates after 1 day. All these findings provide new information to further the understanding of molecular processes involved in iron biomineralization by anaerobic iron-oxidizing bacteria and offer potential signatures of those metabolisms that can be looked for in the geological record. © 2008 Elsevier Ltd. All rights reserved.

Original language	English
Title of host publication	Geochimica et Cosmochimica Acta
Number of pages	16
Publication date	1 Feb 2009
Pages	696-711
ISBN (Print)	0016-7037
DOIs	https://doi.org/10.1016/j.gca.2008.10.033
Publication status	Published - 1 Feb 2009

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title = "Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria",

abstract = "Minerals formed by bio-oxidation of ferrous iron (Fe(II)) at neutral pH, their association with bacterial ultrastructures as well as their impact on the metabolism of iron-oxidizing bacteria remain poorly understood. Here, we investigated iron biomineralization by the anaerobic nitrate-dependent iron-oxidizing bacterium Acidovorax sp. strain BoFeN1 in the presence of dissolved Fe(II) using electron microscopy and Scanning Transmission X-ray Microscopy (STXM). All detected minerals consisted mainly of amorphous iron phosphates, but based on their morphology and localization, three types of precipitates could be discriminated: (1) mineralized filaments at distance from the cells, (2) globules of 100 ± 25 nm in diameter, at the cell surface and (3) a 40-nm thick mineralized layer within the periplasm. All of those phases were shown to be intimately associated with organic molecules. Periplasmic encrustation was accompanied by an accumulation of protein moieties. In the same way, exopolysaccharides were associated with the extracellular mineralized filaments. The evolution of cell encrustation was followed by TEM over the time course of a culture: cell encrustation proceeded progressively, with rapid precipitation in the periplasm (in a few tens of minutes), followed by the formation of surface-bound globules. Moreover, we frequently observed an asymmetric mineral thickening at the cell poles. In parallel, the evolution of iron oxidation was quantified by STXM: iron both contained in the bacteria and in the extracellular precipitates reached complete oxidation within 6 days. While a progressive oxidation of Fe in the bacteria and in the medium could be observed, spatial redox (oxido-reduction state) heterogeneities were detected at the cell poles and in the extracellular precipitates after 1 day. All these findings provide new information to further the understanding of molecular processes involved in iron biomineralization by anaerobic iron-oxidizing bacteria and offer potential signatures of those metabolisms that can be looked for in the geological record. {\textcopyright} 2008 Elsevier Ltd. All rights reserved.",

author = "Jennyfer Miot and Karim Benzerara and Guillaume Morin and Andreas Kappler and Sylvain Bernard and Martin Obst and C{\'e}line F{\'e}rard and F{\'e}riel Skouri-Panet and Guigner, {Jean Michel} and Nicole Posth and Matthieu Galvez and Brown, {Gordon E.} and Fran{\c c}ois Guyot",

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AU - Miot, Jennyfer

AU - Benzerara, Karim

AU - Morin, Guillaume

AU - Kappler, Andreas

AU - Bernard, Sylvain

AU - Obst, Martin

AU - Férard, Céline

AU - Skouri-Panet, Fériel

AU - Guigner, Jean Michel

AU - Posth, Nicole

AU - Galvez, Matthieu

AU - Brown, Gordon E.

AU - Guyot, François

PY - 2009/2/1

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N2 - Minerals formed by bio-oxidation of ferrous iron (Fe(II)) at neutral pH, their association with bacterial ultrastructures as well as their impact on the metabolism of iron-oxidizing bacteria remain poorly understood. Here, we investigated iron biomineralization by the anaerobic nitrate-dependent iron-oxidizing bacterium Acidovorax sp. strain BoFeN1 in the presence of dissolved Fe(II) using electron microscopy and Scanning Transmission X-ray Microscopy (STXM). All detected minerals consisted mainly of amorphous iron phosphates, but based on their morphology and localization, three types of precipitates could be discriminated: (1) mineralized filaments at distance from the cells, (2) globules of 100 ± 25 nm in diameter, at the cell surface and (3) a 40-nm thick mineralized layer within the periplasm. All of those phases were shown to be intimately associated with organic molecules. Periplasmic encrustation was accompanied by an accumulation of protein moieties. In the same way, exopolysaccharides were associated with the extracellular mineralized filaments. The evolution of cell encrustation was followed by TEM over the time course of a culture: cell encrustation proceeded progressively, with rapid precipitation in the periplasm (in a few tens of minutes), followed by the formation of surface-bound globules. Moreover, we frequently observed an asymmetric mineral thickening at the cell poles. In parallel, the evolution of iron oxidation was quantified by STXM: iron both contained in the bacteria and in the extracellular precipitates reached complete oxidation within 6 days. While a progressive oxidation of Fe in the bacteria and in the medium could be observed, spatial redox (oxido-reduction state) heterogeneities were detected at the cell poles and in the extracellular precipitates after 1 day. All these findings provide new information to further the understanding of molecular processes involved in iron biomineralization by anaerobic iron-oxidizing bacteria and offer potential signatures of those metabolisms that can be looked for in the geological record. © 2008 Elsevier Ltd. All rights reserved.

AB - Minerals formed by bio-oxidation of ferrous iron (Fe(II)) at neutral pH, their association with bacterial ultrastructures as well as their impact on the metabolism of iron-oxidizing bacteria remain poorly understood. Here, we investigated iron biomineralization by the anaerobic nitrate-dependent iron-oxidizing bacterium Acidovorax sp. strain BoFeN1 in the presence of dissolved Fe(II) using electron microscopy and Scanning Transmission X-ray Microscopy (STXM). All detected minerals consisted mainly of amorphous iron phosphates, but based on their morphology and localization, three types of precipitates could be discriminated: (1) mineralized filaments at distance from the cells, (2) globules of 100 ± 25 nm in diameter, at the cell surface and (3) a 40-nm thick mineralized layer within the periplasm. All of those phases were shown to be intimately associated with organic molecules. Periplasmic encrustation was accompanied by an accumulation of protein moieties. In the same way, exopolysaccharides were associated with the extracellular mineralized filaments. The evolution of cell encrustation was followed by TEM over the time course of a culture: cell encrustation proceeded progressively, with rapid precipitation in the periplasm (in a few tens of minutes), followed by the formation of surface-bound globules. Moreover, we frequently observed an asymmetric mineral thickening at the cell poles. In parallel, the evolution of iron oxidation was quantified by STXM: iron both contained in the bacteria and in the extracellular precipitates reached complete oxidation within 6 days. While a progressive oxidation of Fe in the bacteria and in the medium could be observed, spatial redox (oxido-reduction state) heterogeneities were detected at the cell poles and in the extracellular precipitates after 1 day. All these findings provide new information to further the understanding of molecular processes involved in iron biomineralization by anaerobic iron-oxidizing bacteria and offer potential signatures of those metabolisms that can be looked for in the geological record. © 2008 Elsevier Ltd. All rights reserved.

U2 - 10.1016/j.gca.2008.10.033

DO - 10.1016/j.gca.2008.10.033

M3 - Book chapter

SN - 0016-7037

SP - 696

EP - 711

BT - Geochimica et Cosmochimica Acta

ER -

Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria

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