Forced Biomineralization: A Review

Abstract

Biologically induced and controlled mineralization of metals promotes the development of protective structures to shield cells from thermal, chemical, and ultraviolet stresses. Metal biomineralization is widely considered to have been relevant for the survival of life in the environmental conditions of ancient terrestrial oceans. Similar behavior is seen among extremophilic biomineralizers today, which have evolved to inhabit a variety of industrial aqueous environments with elevated metal concentrations. As an example of extreme biomineralization, we introduce the category of "forced biomineralization", which we use to refer to the biologically mediated sequestration of dissolved metals and metalloids into minerals. We discuss forced mineralization as it is known to be carried out by a variety of organisms, including polyextremophiles in a range of psychrophilic, thermophilic, anaerobic, alkaliphilic, acidophilic, and halophilic conditions, as well as in environments with very high or toxic metal ion concentrations. While much additional work lies ahead to characterize the various pathways by which these biominerals form, forced biomineralization has been shown to provide insights for the progression of extreme biomimetics, allowing for promising new forays into creating the next generation of composites using organic-templating approaches under biologically extreme laboratory conditions relevant to a wide range of industrial conditions.

Keywords: biomineralization; extreme biomimetics; extreme environments; polyextremophiles.

Figure 1

Transmission electron micrograph of a Cupriavidus metallidurans ultra-thin section containing a gold nano-particle (white arrow) in the periplasm. Reproduced from [53] with permission of PNAS, Copyright 2009 National Academy of Sciences.

Figure 2

(a) Structure of defltibactin A, (b) Gallium NMR confirms that delftibactin has a single metal-binding site. (c) TEM of delftibactin–gold (2:1) complex after 10 min reveals the presence of colloidal and octahedral gold nanoparticles, reminiscent of those seen in natural deposits. Blue arrow, colloidal gold. Red arrow, octahedral gold. (Scale bar 50 nm). Reprinted with permission from Macmillan Publishers Ltd: Nature Chemical Biology [55], copyright 2013.

Figure 3

The chemical structure of glycine-Cr(III) as a proposed precursor for hydrothermal crystallization of α-CrOOH (grimaldiite) and β-CrOOH (guyanaite) at 250 °C. Adapted from Cheng et al. [151].

Figure 4

(a,b) SEM micrographs of mat and crust material from the Ula Nui hydrothermal vent area show diverse Fe-containing structures. The banding patterns of unusual nanoparticle morphologies observed are thought to be of biogenic origin but have not been reported elsewhere. Scale bar 1 µm. (Reprinted by permission from Macmillan Publishers Ltd: The ISME Journal [194], copyright 2011).

Figure 5

Formation of irregular Te(0) “nanospheres” by Sulfurospirillum barnesii. (a) Whole-mount TEM image of a single cell grown on Te(VI), showing abundant external Te nanospheres (small arrows) forming larger aggregates (large arrow) on the cell surfaces. (b) Lower-magnification TEM image of another single cell grown on Te(VI) showing abundant external Te nanospheres. (c) Wide-field SEM image of the Te(0) nanosphere aggregates formed after growth on Te(VI). (d) Unstained TEM thin-section image of cells grown on Te(VI) showing internal accumulations of Te(0). (e) SEM image of Te(0) obtained from a chemical supply house. Reproduced from [211] with permission from the American Society for Microbiology.