title: Fe biomineralization mirrors individual metabolic activity in a nitrate-dependent Fe(II)-oxidizer.
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.
authors.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.
authors.forename: Jennyfer
authors.initials: J
authors.lastname: Miot
authors.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.
authors.forename: Laurent
authors.initials: L
authors.lastname: Remusat
authors.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.
authors.forename: Elodie
authors.initials: E
authors.lastname: Duprat
authors.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.
authors.forename: Adriana
authors.initials: A
authors.lastname: Gonzalez
authors.affiliation: Département des Collections, Muséum National d'Histoire Naturelle Paris, France.
authors.forename: Sylvain
authors.initials: S
authors.lastname: Pont
authors.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.
authors.forename: Mélanie
authors.initials: M
authors.lastname: Poinsot
keywords: NanoSIMS; biomoineralization; nitrate dependent ferrous oxidation; phenotypic heterogeneity; viability