Experimental assessment of occurrences and stability of lead-bearing minerals in bacterial biofilms

Abstract

Bio-induced precipitation of lead-bearing minerals is investigated in bacterial biofilms grown by Shewanella oneidensis MR-1 under aerobic conditions. Under the different conditions investigated, thermodynamic calculations establish that the stable mineral phases expected to precipitate are either wulfenite PbMoO 4 or cerussite PbCO 3. However, observations by electron microscopy show that the first solids precipitated within hours at the experimental solution/biofilm interface are crystals of about 20 nm in diameter of pyromorphite Pb 5 (PO 4) 3 (OH,Cl). In Mo-bearing systems, the precipitation of the thermodynamicallypredicted wulfenite phase is delayed compared to the abiotic experiment and is observed only after 7 days of lead exposure. The initial lead phosphate crystals observed on the extracellular polymeric substances are assumed to result from concurrent local abundances of adsorbed Pb 2+ ions and phosphate groups released by metabolically active cells. Scanning electron microscopy observations of samples milled by focused ion beam reveal effective diffusionlimited precipitation of pyromorphite within the well-preserved biofilm porosity.

How Microbial Biofilms Control the Environmental Fate of Engineered Nanoparticles?

“…This has been reported for S. oneidensis MR1 biofilms simultaneously exposed to lead and molybdenum. In this case, although thermodynamics calculations predicted the formation of wulfenite (PbMoO 4 ) only, a fast precipitation of nanoscale pyromorphite crystals was observed in hot spots distributed within the biofilm thickness, while wulfenite production was observed only after 7 days of exposure to lead (Couasnon et al, 2019). Another example concerns Sulfate-Reducing bacteria (SRB), mentioned before, that are known to play a major role in the precipitation of metal sulfide minerals through the reduction of sulfate to sulfide.…”

“…Consequently, because of their metabolic activities, microorganisms within these structures create and maintain micro-environments that are intrinsically different from the surrounding bulk solution (Figure 1). As a result, they impose concentration gradients for organic or inorganic compounds such as phosphate (Couasnon et al, 2019), enzymes or EPS (Flemming and Wingender, 2010), as well as physico-chemical gradients (pH, Eh, pO 2 . .…”

“…For example, these microbial structures can drive ENPs dissolution under low pH or high complexing ligands concentrations (ligand-assisted dissolution) but can also stabilize ENPs surfaces. Conversely, biofilms are also able to impose local oversaturations relative to mineral phases (Finlay et al, 1999;Templeton et al, 2003b;Nancharaiah et al, 2010;Couasnon et al, 2019), that were kept undersaturated in the overlying bulk solution, resulting in the formation of incidental NPs. As a result, biofilms may constitute an important accumulator for ENPs or a source of incidental NPs that can strongly impact their fate through a number of bio-physico-chemical processes that will be discussed in this review.…”

“…To this perspective, another critical factor that needs to be considered is the transformation that ENPs can undergo when in contact with these biological structures (Holden et al, 2016). At a first approximation, ENPs potential for speciation changes could be considered similar to that of free metals that are subjected to strong chemical modifications in biofilms (Templeton et al, 2003a;Couasnon et al, 2019). It is thus likely that ENPs experience similar transformations, driven by the high reactivity of local microenvironments and the important functional sites density spread within the biofilm thickness.…”

“…Existence of gradients in pH or redox state are both reported, and take place at very short spatial scales within the biofilm structure (Yu and Bishop, 2001;Billings et al, 2015;Flemming et al, 2016;Kataky and Knowles, 2018). However, despite their importance, the nature and properties of such microenvironments are still poorly known regarding ligands or metal(loid)s concentrations, even if few studies suggest strong and dynamic changes in local physico-chemical conditions (Couasnon et al, 2019). Nonetheless, it can be anticipated that these "hot spots" of high reactivity exhibit low pHs, important redox changes, and locally concentrate to high extent siderophores and other complexing ligands as well as enzymes.…”