Ecological resource competition as a driver of metallome evolution

The oldest nitrogenase isozyme, emerging a billion years or more before the Great Oxidation Event (GOE), required a molybdenum (Mo)-based cofactor. "Alternative" nitrogenases using iron (Fe) or vanadium (V) cofactors evolved only after the GOE. This history is puzzling because environmental Fe availability decreased after the GOE, while Mo availability increased, due to the contrasting environmental redox behaviors of these elements. Why, then, did the alternatives emerge only after the GOE? Using a model constrained by known microbial Mo quotas, we demonstrate that a strong selection pressure for the use of metals in nitrogenase other than Mo is a plausible consequence of competition between nitrogen-fixing prokaryotes and nitrate-reducing microbes, which require Mo for nitrate reduction and assimilation. This competition would have intensified after the GOE due to increasing availability of nitrate, explaining the evolutionary timing of nitrogenases isozymes. Ecological resource competition therefore emerges as a third driver of metallome evolution in deep-time, alongside the relative environmental availabilities and adaptive advantages of particular metals.