Insight into the evolution of the iron oxidation pathways

Abstract

Iron is a ubiquitous element in the universe. Ferrous iron (Fe(II)) was abundant in the primordial ocean until the oxygenation of the Earth's atmosphere led to its widespread oxidation and precipitation. This change of iron bioavailability likely put selective pressure on the evolution of life. This element is essential to most extant life forms and is an important cofactor in many redox-active proteins involved in a number of vital pathways. In addition, iron plays a central role in many environments as an energy source for some microorganisms. This review is focused on Fe(II) oxidation. The fact that the ability to oxidize Fe(II) is widely distributed in Bacteria and Archaea and in a number of quite different biotopes suggests that the dissimilatory Fe(II) oxidation is an ancient energy metabolism. Based on what is known today about Fe(II) oxidation pathways, we propose that they arose independently more than once in evolution and evolved convergently. The iron paleochemistry, the phylogeny, the physiology of the iron oxidizers, and the nature of the cofactors of the redox proteins involved in these pathways suggest a possible scenario for the timescale in which each type of Fe(II) oxidation pathways evolved. The nitrate dependent anoxic iron oxidizers are likely the most ancient iron oxidizers. We suggest that the phototrophic anoxic iron oxidizers arose in surface waters after the Archaea/Bacteria-split but before the Great Oxidation Event. The neutrophilic oxic iron oxidizers possibly appeared in microaerobic marine environments prior to the Great Oxidation Event while the acidophilic ones emerged likely after the advent of atmospheric O2. This article is part of a Special Issue entitled: The evolutionary aspects of bioenergetic systems.