Limits...
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

(A)13C14N/12C14N ratio distributions as deduced from NanoSIMS analyses in mineralized (gray) vs. non-mineralized (white) populations from cultures grown for 4 days (tmin = 4 days) in different biomineralization media (Lp-, Mt-, FeP-, Gt-) then transferred to labeled medium for 4 days (tlab = 4 days). (B) Evolution of 13C14N/12C14N ratio distributions with increasing time of mineralization (Gt-medium), determined by NanoSIMS analyses of single mineralized (gray) vs. non-mineralized (white) cells in cultures incubated for 4 days in the labeled medium (tlab = 4 days). (A,B) For a given distribution, the box boundaries indicate the first and third quartiles; the bold band inside the box corresponds to the median value. The vertical lines that extend from the box encompass the largest/smallest observation that falls within a distance of 1.5 times the box size from the nearest box hinge. Outliers are shown separately (individual points).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4562303&req=5

Figure 7: (A)13C14N/12C14N ratio distributions as deduced from NanoSIMS analyses in mineralized (gray) vs. non-mineralized (white) populations from cultures grown for 4 days (tmin = 4 days) in different biomineralization media (Lp-, Mt-, FeP-, Gt-) then transferred to labeled medium for 4 days (tlab = 4 days). (B) Evolution of 13C14N/12C14N ratio distributions with increasing time of mineralization (Gt-medium), determined by NanoSIMS analyses of single mineralized (gray) vs. non-mineralized (white) cells in cultures incubated for 4 days in the labeled medium (tlab = 4 days). (A,B) For a given distribution, the box boundaries indicate the first and third quartiles; the bold band inside the box corresponds to the median value. The vertical lines that extend from the box encompass the largest/smallest observation that falls within a distance of 1.5 times the box size from the nearest box hinge. Outliers are shown separately (individual points).

Mentions: This trend is confirmed by the plots displaying 13C14N/12C14N as a function of 16O/CN in the different samples that were exposed for 4 days to biomineralization conditions before being transferred to the labeled medium (for 4 h, 1 day or 4 days; Figure 6). Within each sample, most of the mineralized cells exhibit a lower 13C14N/12C14N ratio than non-mineralized cells. Mean 13C14N/12C14N ratios have been calculated and compared for each subpopulation (mineralized vs. non-mineralized cells) of each sample (Figure 7). After 4 days of biomineralization (in Lp, FeP, or Gt media) followed by 4 days in the labeled medium, mineralized cells from a given sample incorporated significantly less acetate than non-mineralized cells from the same sample (Figure 7A). Noteworthy, mineralized cells exhibited comparable 13C14N/12C14N distributions, whatever the composition of the biomineralization medium they came from.


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)

(A)13C14N/12C14N ratio distributions as deduced from NanoSIMS analyses in mineralized (gray) vs. non-mineralized (white) populations from cultures grown for 4 days (tmin = 4 days) in different biomineralization media (Lp-, Mt-, FeP-, Gt-) then transferred to labeled medium for 4 days (tlab = 4 days). (B) Evolution of 13C14N/12C14N ratio distributions with increasing time of mineralization (Gt-medium), determined by NanoSIMS analyses of single mineralized (gray) vs. non-mineralized (white) cells in cultures incubated for 4 days in the labeled medium (tlab = 4 days). (A,B) For a given distribution, the box boundaries indicate the first and third quartiles; the bold band inside the box corresponds to the median value. The vertical lines that extend from the box encompass the largest/smallest observation that falls within a distance of 1.5 times the box size from the nearest box hinge. Outliers are shown separately (individual points).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 7: (A)13C14N/12C14N ratio distributions as deduced from NanoSIMS analyses in mineralized (gray) vs. non-mineralized (white) populations from cultures grown for 4 days (tmin = 4 days) in different biomineralization media (Lp-, Mt-, FeP-, Gt-) then transferred to labeled medium for 4 days (tlab = 4 days). (B) Evolution of 13C14N/12C14N ratio distributions with increasing time of mineralization (Gt-medium), determined by NanoSIMS analyses of single mineralized (gray) vs. non-mineralized (white) cells in cultures incubated for 4 days in the labeled medium (tlab = 4 days). (A,B) For a given distribution, the box boundaries indicate the first and third quartiles; the bold band inside the box corresponds to the median value. The vertical lines that extend from the box encompass the largest/smallest observation that falls within a distance of 1.5 times the box size from the nearest box hinge. Outliers are shown separately (individual points).
Mentions: This trend is confirmed by the plots displaying 13C14N/12C14N as a function of 16O/CN in the different samples that were exposed for 4 days to biomineralization conditions before being transferred to the labeled medium (for 4 h, 1 day or 4 days; Figure 6). Within each sample, most of the mineralized cells exhibit a lower 13C14N/12C14N ratio than non-mineralized cells. Mean 13C14N/12C14N ratios have been calculated and compared for each subpopulation (mineralized vs. non-mineralized cells) of each sample (Figure 7). After 4 days of biomineralization (in Lp, FeP, or Gt media) followed by 4 days in the labeled medium, mineralized cells from a given sample incorporated significantly less acetate than non-mineralized cells from the same sample (Figure 7A). Noteworthy, mineralized cells exhibited comparable 13C14N/12C14N distributions, whatever the composition of the biomineralization medium they came from.

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