Membrane Vesicles as a Novel Strategy for Shedding Encrusted Cell Surfaces

Shao, Paul; Comolli, Luis R.; Bernier‐Latmani, Rizlan

doi:10.3390/min4010074

Cited by 23 publications

(18 citation statements)

References 52 publications

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“…Makarova et al 33 demonstrated that metal oxidation reactions, particularly with Fe, ultimately denature S-layer proteins. Membrane vesicle release may therefore be seen as an attempt by Sulfolobus cells to eliminate damaged S-layer proteins in order to enable replacement with new proteins (not associated with minerals), in a manner similar to that seen in organisms lacking S-layers for elimination of denatured or mineral-associated cell wall components 45 46 . Based on our present results, this issue of cell viability and response to stress upon passive Fe biomineralization would deserve a dedicated study.…”

Section: Discussionmentioning

confidence: 99%

Preservation of Archaeal Surface Layer Structure During Mineralization

Kish

Miot

Lombard

et al. 2016

Sci Rep

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Proteinaceous surface layers (S-layers) are highly ordered, crystalline structures commonly found in prokaryotic cell envelopes that augment their structural stability and modify interactions with metals in the environment. While mineral formation associated with S-layers has previously been noted, the mechanisms were unconstrained. Using Sulfolobus acidocaldarius a hyperthermophilic archaeon native to metal-enriched environments and possessing a cell envelope composed only of a S-layer and a lipid cell membrane, we describe a passive process of iron phosphate nucleation and growth within the S-layer of cells and cell-free S-layer “ghosts” during incubation in a Fe-rich medium, independently of metabolic activity. This process followed five steps: (1) initial formation of mineral patches associated with S-layer; (2) patch expansion; (3) patch connection; (4) formation of a continuous mineral encrusted layer at the cell surface; (5) early stages of S-layer fossilization via growth of the extracellular mineralized layer and the mineralization of cytosolic face of the cell membrane. At more advanced stages of encrustation, encrusted outer membrane vesicles are formed, likely in an attempt to remove damaged S-layer proteins. The S-layer structure remains strikingly well preserved even upon the final step of encrustation, offering potential biosignatures to be looked for in the fossil record.

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Section: Discussionmentioning

confidence: 99%

Preservation of Archaeal Surface Layer Structure During Mineralization

Kish

Miot

Lombard

et al. 2016

Sci Rep

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“…As mentioned above, vesiculation functions as an envelope stress response, and increasing OMV production aids in bacterial survival under stress conditions 19,20,22,24–27,42,75,76 (FIG. 3a, b).…”

Section: Omv Functions In Bacterial Physiologymentioning

confidence: 99%

Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions

2015

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Outer-membrane vesicles (OMVs) are spherical buds of the outer membrane filled with periplasmic content and are commonly produced by Gram-negative bacteria. The production of OMVs allows bacteria to interact with their environment, and OMVs have been found to mediate diverse functions, including promoting pathogenesis, enabling bacterial survival during stress conditions and regulating microbial interactions within bacterial communities. Additionally, because of this functional versatility, researchers have begun to explore OMVs as a platform for bioengineering applications. In this Review, we discuss recent advances in the study of OMVs, focusing on new insights into the mechanisms of biogenesis and the functions of these vesicles.

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“…This has been shown in stromatolites ( Decho et al, 2005 ) and in other systems, among which Fe cycling bacteria. For instance, EPS are produced by the Fe(III)-reducer Shewanella oneidensis promoting the precipitation of uraninite ( Shao et al, 2014 ) and by nitrate-dependent iron(II)-oxidizing bacteria precipitating Fe-oxyhydroxides or phosphates ( Miot et al, 2009b ; Klueglein et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

“…Recently, S. oneidensis was shown to form membrane vesicles that get mineralized when exposed to uranium, hence lessening cell surface mineralization ( Shao et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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

Miot¹,

Rémusat²,

Duprat³

et al. 2015

Front. Microbiol.

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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.

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Membrane Vesicles as a Novel Strategy for Shedding Encrusted Cell Surfaces

Cited by 23 publications

References 52 publications

Preservation of Archaeal Surface Layer Structure During Mineralization

Preservation of Archaeal Surface Layer Structure During Mineralization

Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions

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

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