Ecological resource competition as a driver of metallome evolution
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Undoubtedly, Earth’s first redox revolution, which culminated ∼2.4 billion years ago in the Great Oxidation Event (GOE), fundamentally altered the resources available to microbial communities, leading to novel ecological competitions and evolutionary innovations. These eco-evolutionary dynamics are largely unexplored, particularly at the molecular level. Here, we hypothesize that such dynamics in the wake of the GOE explain the otherwise paradoxical evolutionary history of metal use in nitrogen fixation by nitrogenase. This ancient metalloenzyme exists in three isozymes, with distinct metal cofactors. Recent research demonstrates that the most ancient isozyme, emerging a billion years or more before the GOE, required a molybdenum (Mo)-based cofactor. “Alternative” nitrogenases using iron (Fe) or vanadium (V) cofactors evolved after the GOE. This history is puzzling because Mo availability in the environment increased after the GOE, while Fe availability decreased , due to the contrasting environmental redox behaviors of these elements. Why, then, did the alternatives emerge only after the GOE? Using a simple model constrained by known microbial Mo quotas, we demonstrate that a strong selection pressure for use of metals in nitrogenase other than Mo is a likely 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 environmental availability of nitrate, explaining the evolutionary timing of the nitrogenase 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.
Significance statement
The selection of metals in biochemical evolution is widely attributed to either the relative environmental availability of specific metals or their functional benefits in biological systems. We propose a third pressure, ecological resource competition, which is typically overlooked as a driver of molecular novelty in deep time. Specifically, we hypothesize that competition between Mo-dependent nitrogen-fixing prokaryotes and Mo-dependent nitrate reducers led to the emergence of Mo-free “alternative” nitrogenase enzymes during the early Proterozoic. This novel hypothesis explains the paradoxical emergence of alternative nitrogenases after the Great Oxidation Event despite increasing ocean Mo abundances at that time. Competition among microbial species for the same metals likely drove molecular innovations, especially in response to dynamically changing geochemical landscapes.
