Inhibition of photoferrotrophy by nitric oxide in ferruginous environments

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 Archean and Paleoproterozoic (3.8-1.85 Ga) banded iron formations (BIF). The end of BIF deposition by photoferrotrophs has often been interpreted as being the result a deepening of water column oxygenation below the photic zone concomitant with the proliferation of cyanobacteria. We suggest here that a potentially overlooked aspect influencing BIF precipitation by photoferrotrophs is competition with another anaerobic Fe(II)-oxidizing metabolism. It is speculated that microorganisms capable of coupling Fe(II) oxidation to the reduction of nitrate were also present early in Earth history when BIF were being deposited, but the extent to which they could compete with photoferrotrophs when favourable geochemical conditions overlapped is unknown. Utilizing microbial incubations and numerical modelling, we show that nitrate-reducing Fe(II)-oxidizers metabolically outcompete photoferrotrophs for dissolved Fe(II). Moreover, the nitrate-reducing Fe(II)-oxidizers inhibit photoferrotrophy via the production of toxic nitric oxide (NO). Four different photoferrotrophs, representing both green sulfur and purple non-sulfur bacteria, are susceptible to this toxic effect despite having genomic capabilities for NO detoxification. Indeed, despite NO detoxification mechanisms being ubiquitous in some groups of phototrophs at the genomic level (e.g. Chlorobi and Cyanobacteria) it is likely they would still be influenced by NO stress. We suggest that the production of NO during nitrate-reducing Fe(II) oxidation in ferruginous environments represents an as yet unreported control on the activity of photoferrotrophs in the ancient oceans and thus the mechanisms driving precipitation of BIF.