Abstract
Surface encrustation by minerals, which impedes cellular metabolism, is a potential hazard for microbes. The reduction of U(VI) to U(IV) by Shewanella oneidensis strain MR-1 leads to the precipitation of the mineral uraninite, as well as a non-crystalline U(IV) product. The wild-type (WT) strain can produce extracellular polymeric substances (EPS), prompting precipitation of U some distance from the cells and precluding encrustation. Using cryo-transmission electron microscopy and scanning transmission X-ray microscopy we show that, in the biofilm-deficient mutant ∆mxdA, as well as in the WT strain to a lesser extent, we observe the formation of membrane vesicles (MVs) as an additional means to lessen encrustation. Additionally, under conditions in which the WT does not produce EPS, formation of MVs was the only observed mechanism to mitigate cell encrustation. Viability studies comparing U-free controls to cells exposed to U showed a decrease in the number of viable cells in conditions where MVs alone are detected, yet no loss of viability when cells produce both EPS and MVs. We conclude that MV formation is a microbial strategy to shed encrusted cell surfaces but is less effective at maintaining cell viability than the precipitation of U on EPS.
Highlights
Microbes living in an environment containing metals are exposed to biotic and abiotic reactions that can result in nucleation of minerals on their outer surface [1,2]
Our results show that membrane vesicles (MVs) formation benefits the cells to some extent for the preservation of viability in cells challenged with U
In cells incubated in the absence of U, no evidence for MV formation was uncovered (Figure 3), while in cells exposed to U, the contribution of MVs was always noticeable (Figures 1, 5 and 6)
Summary
Microbes living in an environment containing metals are exposed to biotic and abiotic reactions that can result in nucleation of minerals on their outer surface [1,2]. A number of mechanisms to minimize encrustation have been identified primarily for Fe(II)-oxidizing bacteria [9] and include the localization of metal sorption or precipitation on extracellular structures some distance for the cells [2,10], the solubilization of minerals by modifying the pH microenvironment around the cell [2,11], and/or altering surface charge properties [12,13]. These microorganisms are likely to employ a combination of these strategies to prevent encrustation
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