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Fe biomineralization mirrors individual metabolic activity in a nitrate-dependent Fe(II)-oxidizer.

Miot J, Remusat L, Duprat E, Gonzalez A, Pont S, Poinsot M - Front Microbiol (2015)

Bottom Line: Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall.Carbon assimilation decreased exponentially with increasing cell-associated Fe content.Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples.

View Article: PubMed Central - PubMed

Affiliation: Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Muséum National d'Histoire Naturelle, Université Pierre et Marie Curie - Sorbonne Universités, CNRS UMR 7590, IRD 206 Paris, France.

ABSTRACT
Microbial biomineralization sometimes leads to periplasmic encrustation, which is predicted to enhance microorganism preservation in the fossil record. Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall. This hypothesis had, however, never been investigated down to the single cell level. Here, we cultured the nitrate reducing Fe(II) oxidizing bacteria Acidovorax sp. strain BoFeN1 that have been previously shown to promote the precipitation of a diversity of Fe minerals (lepidocrocite, goethite, Fe phosphate) encrusting the periplasm. We investigated the connection of Fe biomineralization with carbon assimilation at the single cell level, using a combination of electron microscopy and Nano-Secondary Ion Mass Spectrometry. Our analyses revealed strong individual heterogeneities of Fe biomineralization. Noteworthy, a small proportion of cells remaining free of any precipitate persisted even at advanced stages of biomineralization. Using pulse chase experiments with (13)C-acetate, we provide evidence of individual phenotypic heterogeneities of carbon assimilation, correlated with the level of Fe biomineralization. Whereas non- and moderately encrusted cells were able to assimilate acetate, higher levels of periplasmic encrustation prevented any carbon incorporation. Carbon assimilation only depended on the level of Fe encrustation and not on the nature of Fe minerals precipitated in the cell wall. Carbon assimilation decreased exponentially with increasing cell-associated Fe content. Persistence of a small proportion of non-mineralized and metabolically active cells might constitute a survival strategy in highly ferruginous environments. Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples.

No MeSH data available.


Related in: MedlinePlus

Electron microscopy analysis of BoFeN1 cells cultured in the different biomineralization media: (A,B); Lp-, (C,D); Mt-, (E,F); FeP- and (G,H); Gt-media. (A,C,E,G) are TEM images and (B,D,F,H) are scanning electron microscopy (SEM) images in secondary electron mode. Insets display corresponding selected area electron diffraction (SAED) patterns of lepidocrocite (A), magnetite (C), amorphous Fe-phosphate (E), and goethite (G). White and orange arrows indicate non-encrusted vs. encrusted cells, respectively.
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Figure 1: Electron microscopy analysis of BoFeN1 cells cultured in the different biomineralization media: (A,B); Lp-, (C,D); Mt-, (E,F); FeP- and (G,H); Gt-media. (A,C,E,G) are TEM images and (B,D,F,H) are scanning electron microscopy (SEM) images in secondary electron mode. Insets display corresponding selected area electron diffraction (SAED) patterns of lepidocrocite (A), magnetite (C), amorphous Fe-phosphate (E), and goethite (G). White and orange arrows indicate non-encrusted vs. encrusted cells, respectively.

Mentions: In biomineralization media, BoFeN1 cells get encrusted with Fe-minerals. As previously described, different minerals are produced depending on the medium composition and the nature of Fe source (Kappler et al., 2005; Miot et al., 2009a,b, 2014a,b; Pantke et al., 2012). In a pH neutral medium without phosphate (Lp-medium), lepidocrocite is precipitated in the periplasm as well as in the extracellular medium [Figure 1A, (Miot et al., 2014b)]. At pH 8, green rust precipitates as long as nitrate is added to the medium. Bacteria further transform green rust and dissolved Fe(II) into extracellular magnetite and periplasmic lepidocrocite [Mt-medium, Figure 1C, (Miot et al., 2014a)]. In the presence of 1 mM phosphate and 5 mM Fe (FeP-medium), amorphous Fe phosphate is precipitated in the periplasm as well as at the cell surface [Figure 1E, (Miot et al., 2009a)]. At lower phosphate concentrations (<1 mM; Gt-medium), goethite precipitates both in the periplasm and at the cell contact [Figure 1G, (Pantke et al., 2012)]. Hence, whatever the composition of the biomineralization medium, periplasmic precipitation of Fe-minerals is observed, whereas extracellular precipitation of Fe-bearing phases is more or less extensive depending on the chemical conditions. After biomineralization, cells have been transferred to a labeled medium. This labeled medium did not contain iron thus could not promote any further biomineralization.


Fe biomineralization mirrors individual metabolic activity in a nitrate-dependent Fe(II)-oxidizer.

Miot J, Remusat L, Duprat E, Gonzalez A, Pont S, Poinsot M - Front Microbiol (2015)

Electron microscopy analysis of BoFeN1 cells cultured in the different biomineralization media: (A,B); Lp-, (C,D); Mt-, (E,F); FeP- and (G,H); Gt-media. (A,C,E,G) are TEM images and (B,D,F,H) are scanning electron microscopy (SEM) images in secondary electron mode. Insets display corresponding selected area electron diffraction (SAED) patterns of lepidocrocite (A), magnetite (C), amorphous Fe-phosphate (E), and goethite (G). White and orange arrows indicate non-encrusted vs. encrusted cells, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4562303&req=5

Figure 1: Electron microscopy analysis of BoFeN1 cells cultured in the different biomineralization media: (A,B); Lp-, (C,D); Mt-, (E,F); FeP- and (G,H); Gt-media. (A,C,E,G) are TEM images and (B,D,F,H) are scanning electron microscopy (SEM) images in secondary electron mode. Insets display corresponding selected area electron diffraction (SAED) patterns of lepidocrocite (A), magnetite (C), amorphous Fe-phosphate (E), and goethite (G). White and orange arrows indicate non-encrusted vs. encrusted cells, respectively.
Mentions: In biomineralization media, BoFeN1 cells get encrusted with Fe-minerals. As previously described, different minerals are produced depending on the medium composition and the nature of Fe source (Kappler et al., 2005; Miot et al., 2009a,b, 2014a,b; Pantke et al., 2012). In a pH neutral medium without phosphate (Lp-medium), lepidocrocite is precipitated in the periplasm as well as in the extracellular medium [Figure 1A, (Miot et al., 2014b)]. At pH 8, green rust precipitates as long as nitrate is added to the medium. Bacteria further transform green rust and dissolved Fe(II) into extracellular magnetite and periplasmic lepidocrocite [Mt-medium, Figure 1C, (Miot et al., 2014a)]. In the presence of 1 mM phosphate and 5 mM Fe (FeP-medium), amorphous Fe phosphate is precipitated in the periplasm as well as at the cell surface [Figure 1E, (Miot et al., 2009a)]. At lower phosphate concentrations (<1 mM; Gt-medium), goethite precipitates both in the periplasm and at the cell contact [Figure 1G, (Pantke et al., 2012)]. Hence, whatever the composition of the biomineralization medium, periplasmic precipitation of Fe-minerals is observed, whereas extracellular precipitation of Fe-bearing phases is more or less extensive depending on the chemical conditions. After biomineralization, cells have been transferred to a labeled medium. This labeled medium did not contain iron thus could not promote any further biomineralization.

Bottom Line: Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall.Carbon assimilation decreased exponentially with increasing cell-associated Fe content.Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples.

View Article: PubMed Central - PubMed

Affiliation: Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Muséum National d'Histoire Naturelle, Université Pierre et Marie Curie - Sorbonne Universités, CNRS UMR 7590, IRD 206 Paris, France.

ABSTRACT
Microbial biomineralization sometimes leads to periplasmic encrustation, which is predicted to enhance microorganism preservation in the fossil record. Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall. This hypothesis had, however, never been investigated down to the single cell level. Here, we cultured the nitrate reducing Fe(II) oxidizing bacteria Acidovorax sp. strain BoFeN1 that have been previously shown to promote the precipitation of a diversity of Fe minerals (lepidocrocite, goethite, Fe phosphate) encrusting the periplasm. We investigated the connection of Fe biomineralization with carbon assimilation at the single cell level, using a combination of electron microscopy and Nano-Secondary Ion Mass Spectrometry. Our analyses revealed strong individual heterogeneities of Fe biomineralization. Noteworthy, a small proportion of cells remaining free of any precipitate persisted even at advanced stages of biomineralization. Using pulse chase experiments with (13)C-acetate, we provide evidence of individual phenotypic heterogeneities of carbon assimilation, correlated with the level of Fe biomineralization. Whereas non- and moderately encrusted cells were able to assimilate acetate, higher levels of periplasmic encrustation prevented any carbon incorporation. Carbon assimilation only depended on the level of Fe encrustation and not on the nature of Fe minerals precipitated in the cell wall. Carbon assimilation decreased exponentially with increasing cell-associated Fe content. Persistence of a small proportion of non-mineralized and metabolically active cells might constitute a survival strategy in highly ferruginous environments. Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples.

No MeSH data available.


Related in: MedlinePlus