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 13C-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.

Microbial anaerobic Fe(II) oxidation – Ecology, mechanisms and environmental implications

“…While some Fe(II)-oxidizing bacteria such as photoferrotrophs and the autotrophic Culture KS have developed strategies for avoiding cell encrustation by Fe(III) minerals (Hegler et al, 2010), no such strategies have been demonstrated by chemodenitrifying bacteria (Schaedler et al, 2009;Klueglein et al, 2014). Cell encrustation inhibits respiratory complexes and other periplasmic sites which leads to decreased nitrate-dependent Fe(II) oxidation (Carlson et al, 2013) and eventually results in cell death (though not always for all community members, e.g., Miot et al, 2015). (Kumaraswamy et al, 2006) and Desulfitobacterium frappieri (Shelobolina et al, 2003).…”

“…For many chemodenitrifiers, precipitation occurs in the periplasm, as shells which completely enclose the cell, or in extracellular globules or as Fe filaments on extracellular polymeric substances (EPS) (Kappler et al, 2005b;Miot et al, 2009b;Schaedler et al, 2009;Schmid et al, 2014). The extent of encrustation increasingly limits the metabolic capabilities of these bacteria until encrustation is so severe that they are killed (Miot et al, 2015). The extent to which encrustation is an artefact caused by high Fe(II) concentrations in lab conditions is unclear, but such structures have been observed in the environment .…”

Substrate and electron donor limitation induce phenotypic heterogeneity in different metabolic activities in a green sulphur bacterium

“…Phenotypic heterogeneity helps microbial populations (Ackermann, 2015) to adapt to fluctuating environmental conditions (Balaban et al, 2004;Kussell and Leibler, 2005;Acar et al, 2008;Beaumont et al, 2009;Ratcliff and Denison, 2010;Arnoldini et al, 2014;Schreiber et al, 2016), aids in the division of labour within isogenic cell populations (Ackermann et al, 2008) and can result from negative frequency-dependent interactions in mixed resource environments (Healey et al, 2016). Multiple studies on phenotypic heterogeneity have been conducted with microbial model strains, while only a few studies have investigated environmental isolates (Ziv et al, 2013;Holland et al, 2014;New et al, 2014;Miot et al, 2015;Guantes et al, 2016) or natural microbial populations Zimmermann et al, 2015;Sheik et al, 2016). Thus, there remains a knowledge gap as to how phenotypic heterogeneity is controlled in environmental bacteria without long laboratory culture history and in natural microbial populations.…”

Microbially mediated aluminosilicate formation in acidic anaerobic environments: A cell‐scale chemical perspective

“…This process would not affect, however, the most soluble cations (e.g., Mg, Mn, Zn, Co, Ni; Table S1), which require significantly higher pH conditions to precipitate (Sánchez-España & Yusta, 2015). Miot et al (2015) have recently shown that bacterial cells can still maintain a significant degree of carbon assimilation and metabolic activity even with an important level of Fe-mineral encrustation. Using a combination of electron microscopy and nanoSIMS, these authors found that there was a maximum extent of periplasmic mineral encrustation above which cells of the nitrate-reducing, Fe(II)-oxidizing bacteria Acidovorax sp.…”