Geobiological feedbacks, oxygen, and the evolution of nitrogenase

Abstract

Biological nitrogen fixation via the activity of nitrogenase is one of the most important biological innovations, allowing for an increase in global productivity that eventually permitted the emergence of higher forms of life. The complex metalloenzyme termed nitrogenase contains complex iron-sulfur cofactors. Three versions of nitrogenase exist that differ mainly by the presence or absence of a heterometal at the active site metal cluster (either Mo or V). Mo-dependent nitrogenase is the most common while V-dependent or heterometal independent (Fe-only) versions are often termed alternative nitrogenases since they have apparent lower activities for N2 reduction and are expressed in the absence of Mo. Phylogenetic data indicates that biological nitrogen fixation emerged in an anaerobic, thermophilic ancestor of hydrogenotrophic methanogens and later diversified via lateral gene transfer into anaerobic bacteria, and eventually aerobic bacteria including Cyanobacteria. Isotopic evidence suggests that nitrogenase activity existed at 3.2 Ga, prior to the advent of oxygenic photosynthesis and rise of oxygen in the atmosphere, implying the presence of favorable environmental conditions for oxygen-sensitive nitrogenase to evolve. Following the proliferation of oxygenic phototrophs, diazotrophic organisms had to develop strategies to protect nitrogenase from oxygen inactivation and generate the right balance of low potential reducing equivalents and cellular energy for growth and nitrogen fixation activity. Here we review the fundamental advances in our understanding of biological nitrogen fixation in the context of the emergence, evolution, and taxonomic distribution of nitrogenase, with an emphasis placed on key events associated with its emergence and diversification from anoxic to oxic environments.