Near‐neutral surface charge and hydrophilicity prevent mineral encrustation of Fe‐oxidizing micro‐organisms

Abstract

Microbial survival in mineralizing environments depends on the ability to evade surface encrustation by minerals, which could obstruct nutrient uptake and waste output. Some organisms localize mineral precipitation away from the cell; however, cell surface properties - charge and hydrophobicity - must also play a role in preventing surface mineralization. This is especially relevant for iron-oxidizing bacteria (FeOB), which face an encrustation threat from both biotic and abiotic mineralization. We used electron microscopy and surface characterization techniques to study the surfaces of two stalk-forming neutrophilic FeOB: the marine Zetaproteobacterium Mariprofundus ferrooxydans PV-1 and the recently isolated freshwater Betaproteobacterium Gallionellales strain R-1. Both organisms lack detectable iron on cell surfaces. Live and azide-inhibited M. ferrooxydans PV-1 cells had small negative zeta potentials (-0.34 to -2.73 mV), over the pH range 4.2-9.4; Gallionellales strain R-1 cells exhibited an even smaller zeta potential (-0.10 to -0.19 mV) over pH 4.2-8.8. Cells have hydrophilic surfaces, according to water contact angle measurements and microbial adhesion to hydrocarbons tests. Thermodynamic and extended Derjaguin-Landau-Verwey-Overbeek (XDLVO) calculations showed that as low charge causes low electrostatic attraction, hydrophilic repulsion dominates cell-mineral interactions. Therefore, we conclude that surface properties help enable these FeOB to survive in highly mineralizing environments. Given both mineral-repelling surface properties and the ability to sequester Fe(III) biominerals in an organomineral stalk, these two FeOB have a well-coordinated system to localize both biotic and abiotic mineral distribution.

Insights into Nitrate-Reducing Fe(II) Oxidation Mechanisms through Analysis of Cell-Mineral Associations, Cell Encrustation, and Mineralogy in the Chemolithoautotrophic Enrichment Culture KS

“…Despite the observed cell-mineral associations, during autotrophic growth of culture KS, we did not observe any cells that were encrusted in Fe minerals. This is in contrast to the reported heavy encrustation of mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria and heterotrophic nitratereducing bacteria in the presence of high Fe(II) concentrations (3,13,38,39). For most of these cultures that show encrustation, it has been suggested that abiotic oxidation of Fe(II) by accumulated nitrite formed during nitrate reduction is responsible for at least some, if not all, of the Fe(II) oxidation (35,40).…”

“…Furthermore, metabolic inactivity as a result of encrustation has been reported (3). While autotrophic phototrophic and autotrophic microaerophilic Fe(II)-oxidizing bacteria can prevent encrustation (36)(37)(38), tight surface coverage of mixotrophic NRFeOB cells is frequently observed in batch cultures (3,9,35,39 …”

Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

“…strain SW2 (20). Third, Saini and Chan (21) showed a near-neutral cell surface charge and hydrophobicity for Mariprofundus ferrooxydans and Gallionella sp., which will decrease binding and precipitation of positively charged iron(III) ions on the cell surface. Fourth, soluble organic ligands which can complex and solubilize Fe(III) have been proposed (15,22).…”

Mechanisms of extracellular S0 globule production and degradation in Chlorobaculum tepidum via dynamic cell–globule interactions

“…This mechanism should also prevent the encrustation of cells by the mineral. For iron-oxidizing microbes, strategies evolved to avoid encrustation include the formation of extracellular structures (Chan et al, 2011), cell surface tuning (Saini & Chan, 2013) and changing cellular microenvironments (Hegler et al, 2010). These strategies work to direct mineral formation away from the cell surface, allowing cells to avoid complete entombment.…”