Inhibition of phototrophic iron oxidation by nitric oxide in ferruginous environments

Abstract

Anoxygenic phototrophic Fe(II) oxidizers (photoferrotrophs) are thought to have thrived in Earth’s ancient ferruginous oceans and played a primary role in the precipitation of Archaean and Palaeoproterozoic (3.8–1.85-billion-year-old) banded iron formations (BIFs). The end of BIF deposition by photoferrotrophs has been interpreted as the result of a deepening of water-column oxygenation below the photic zone, concomitant with the proliferation of cyanobacteria. However, photoferrotrophs may have experienced competition from other anaerobic Fe(II)-oxidizing microorganisms, altering the formation mechanism of BIFs. Here we utilize microbial incubations to show that nitrate-reducing Fe(II) oxidizers metabolically outcompete photoferrotrophs for dissolved Fe(II). Moreover, both experiments and numerical modelling show that the nitrate-reducing Fe(II) oxidizers inhibit photoferrotrophy via the production of toxic intermediates. Four different photoferrotrophs, representing both green sulfur and purple non-sulfur bacteria, are susceptible to this toxic effect despite having genomic capabilities for nitric oxide detoxification. Indeed, despite nitric oxide detoxification mechanisms being ubiquitous in some groups of phototrophs at the genomic level (for example, Chlorobi and Cyanobacteria) it is likely that they would still be affected. We suggest that the production of reactive nitrogen species during nitrate-reducing Fe(II) oxidation in ferruginous environments may have inhibited the activity of photoferrotrophs in the ancient oceans and thus impeded their role in the precipitation of BIFs. Banded iron formation deposition by photoferrotrophic organisms in the early Earth’s oceans may have been inhibited by competition for iron and toxicity from nitrate-reducing microorganisms, according to a microbial incubation and numerical modelling study.