Oxygenic photosynthesis as a protection mechanism for cyanobacteria against iron-encrustation in environments with high Fe2+ concentrations

Abstract

If O2 is available at circumneutral pH, Fe(2+) is rapidly oxidized to Fe(3+), which precipitates as FeO(OH). Neutrophilic iron oxidizing bacteria have evolved mechanisms to prevent self-encrustation in iron. Hitherto, no mechanism has been proposed for cyanobacteria from Fe(2+)-rich environments; these produce O2 but are seldom found encrusted in iron. We used two sets of illuminated reactors connected to two groundwater aquifers with different Fe(2+) concentrations (0.9 μM vs. 26 μM) in the Äspö Hard Rock Laboratory (HRL), Sweden. Cyanobacterial biofilms developed in all reactors and were phylogenetically different between the reactors. Unexpectedly, cyanobacteria growing in the Fe(2+)-poor reactors were encrusted in iron, whereas those in the Fe(2+)-rich reactors were not. In-situ microsensor measurements showed that O2 concentrations and pH near the surface of the cyanobacterial biofilms from the Fe(2+)-rich reactors were much higher than in the overlying water. This was not the case for the biofilms growing at low Fe(2+) concentrations. Measurements with enrichment cultures showed that cyanobacteria from the Fe(2+)-rich environment increased their photosynthesis with increasing Fe(2+) concentrations, whereas those from the low Fe(2+) environment were inhibited at Fe(2+) > 5 μM. Modeling based on in-situ O2 and pH profiles showed that cyanobacteria from the Fe(2+)-rich reactor were not exposed to significant Fe(2+) concentrations. We propose that, due to limited mass transfer, high photosynthetic activity in Fe(2+)-rich environments forms a protective zone where Fe(2+) precipitates abiotically at a non-lethal distance from the cyanobacteria. This mechanism sheds new light on the possible role of cyanobacteria in precipitation of banded iron formations.