Formation of Cell-Iron-Mineral Aggregates by Phototrophic and Nitrate-Reducing Anaerobic Fe(II)-Oxidizing Bacteria

Abstract

Microbial anaerobic Fe(II) oxidation at neutral pH produces poorly soluble Fe(III) which is expected to bind to cell surfaces causing cell encrustation and potentially impeding cell metabolism. The challenge for Fe(II)-oxidizing prokaryotes therefore is to avoid encrustation with Fe(III). Using different microscopic techniques we tracked Fe(III) minerals at the cell surface and within cells of phylogenetically distinct phototrophic and nitrate-reducing Fe(II)-oxidizing bacteria. While some strains successfully prevented encrustation others precipitated Fe(III) minerals at the cell surface and in the periplasm. Our results indicate differences in the cellular mechanisms of Fe(II) oxidation, transport of Fe(II)/Fe(III) ions, and Fe(III) mineral precipitation.

Functional Characterization of the FoxE Iron Oxidoreductase from the Photoferrotroph Rhodobacter ferrooxidans SW2

“…However, no strong siderophores were detected in SW2 spent medium, and the energetic cost of producing such a molecule would likely be prohibitive (9). An alternative strategy for keeping Fe(III) soluble is the creation of a low pH microenvironment around the cell to promote precipitation away from the cell both thermodynamically and kinetically (8,9,32). This implies a tight pH control of the iron oxidation step.…”

“…This implies that SW2 has a strategy to prevent Fe(III) precipitation in the periplasm and on the cell surface. Different iron-oxidizing bacteria appear to have different mechanisms to avoid precipitation (8), and some, such as Rhodomicrobium vannielii, cannot escape becoming encrusted by iron minerals (31). Iron chelators produced by the cells have been suggested to solubilize Fe(III), and it is known that the growth of SW2 increases the solubility of Fe(III) in the supernatant of the culture medium (28).…”

“…SW2 has been a subject of studies aiming to understand biologically induced mineralization because ferric (hydr)oxides precipitate away from the cell and no mineral is found inside the cells or encrusting the cell surface (7)(8)(9). It is also known that SW2 utilizes only soluble Fe(II) compounds as the electron source for photoferrotrophy and does not actively dissolve Fe(II) minerals (9), suggesting that iron oxidation does not occur at the cell surface.…”

Membrane Vesicles as a Novel Strategy for Shedding Encrusted Cell Surfaces

“…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.…”

“…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]. Excessive mineral formation on the cell surface can lead to complete cell encrustation, potentially impeding cellular metabolism and limiting the microbe's capacity to interface with its environment.…”