Identifying when microbes biosilicify: The interconnected requirements of acidic pH, colloidal SiO2 and exposed microbial surface

This study demonstrates discernible biosilicification of natural microbial mats through batch laboratory experiments. Identification of the geochemical requirements for this process to occur includes thermodynamically favorable, but sluggish silica reaction kinetics associated with acidic conditions, and the necessity for colloidal silica rather than dissolved silicic acid species. This study provides the first results to bridge the apparent literature discrepancy between widespread, in-situ observations of microbial silicification, and the inability to demonstrate a detectable microbial impact in this process under well-constrained laboratory conditions. We compared the silica scavenging abilities of three natural microbial mats collected from Yellowstone National Park (YNP) hotsprings, relative to those of both abiotic particle (TiO2) and solution controls at constant, near-saturated aqueous silica concentrations, while experimental pH and temperature conditions were varied, using both dissolved and colloidal SiO2 forms. We specifically evaluated three microbial mats sampled from YNP sites all exhibiting saturation with respect to amorphous SiO2, but possessing variable pH and temperature conditions that should reflect differential kinetics (and therefore biological opportunity) relative to silica polymerization: (1) most biologically favorable, acidic-mesophile (AM: pH 3, T = 35 °C); (2) biologically possible, but less opportune, alkaline, mesophile (ALK-M: pH 8, T = 35 °C) and (3) unlikely to be biologically favorable, alkaline-thermophile (ALK-T: pH 8, T = 80 °C). Comparison of field and laboratory results substantiates the requirements for thermodynamically favorable, but kinetically slower SiO2 polymerization conditions. Results show that acidic moderate temperature conditions were required for an observable biosilicification impact. Moreover, they also identified for the first time, the necessity specifically for colloidal silica forms which are surface bound under acidic pH conditions, to distinguish discernible biosilicification compared to mineral particle controls. Results also highlight the important influence of mat surface characteristics in this process, specifically the extent of live, non-mineralized, exposed biological mat surface. Greater colloidal SiO2 scavenging abilities are associated with non-mineralized microbial mat surfaces than with mineral particle surfaces or microbial mat surfaces encrusted with authigenic silica. These results are the first to demonstrate that biosilicification can be a microbially mediated, discernible geobiological process, shedding new light on the longstanding argument in the literature, and opening the door for more sensitive evaluation of this phenomenon in natural systems.