Protection of phototrophic iron(II)-oxidizing bacteria from UV irradiation by biogenic iron(III) minerals: Implications for early Archean banded iron formation

Abstract

On the Archean Earth (4.0–2.5 Ga) the lack of a protective ozone layer meant that harmful ultraviolet radiation (UVR) reached the surface almost unattenuated. For survival, primitive photosynthetic bacteria would have required strategies preventing UV-induced damage to their DNA. At that time, a fraction of the planktonic cells were likely anoxygenic photosynthesizers that oxidized dissolved Fe(II) to Fe(III) during their metabolism. The result of their metabolism was most likely the ferric mineral precursors for the deposition of banded iron formations. Although Fe(III) (oxyhydr)oxide minerals absorb UV radiation while still transmitting higher wavelengths, it is unknown whether minerals produced by Fe(II) oxidizers could have acted as an in situ UVR sunscreen. Here we demonstrate that the anoxygenic phototrophic Fe(II) oxidizers Rhodopseudomonas palustris strain TIE-1 and Rhodobacter ferrooxidans strain SW2 form nanometer-sized grains of ferrihydrite that are loosely attached to the cell surfaces. These biogenic Fe(III) minerals were shown to protect the bacteria from UV-C irradiation, while cells grown in the absence of Fe(II) displayed diminished cell viability as a consequence of damage to their DNA. Importantly, this study implies that primitive Fe(II)-oxidizing bacteria would have been able to produce their own UV screen, enabling them to live in the shallow photic zone of ancient oceans.