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Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review

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Abstract

Biological nitrogen fixation (BNF), a key reaction of the nitrogen cycle, is catalyzed by the enzyme nitrogenase. The best studied isoform of this metalloenzyme requires molybdenum (Mo) at its active center to reduce atmospheric dinitrogen (N2) into bioavailable ammonium. The Mo-dependent nitrogenase is found in all diazotrophs and is the only nitrogenase reported in diazotrophs that form N2-fixing symbioses with higher plants. In addition to the canonical Mo nitrogenase, two alternative nitrogenases, which use either vanadium (V) or iron (Fe) instead of Mo are known to fix nitrogen. They have been identified in ecologically important groups including free-living bacteria in soils and freshwaters and as symbionts of certain cryptogamic covers. Despite the discovery of these alternative isoforms more than 40 years ago, BNF is still believed to primarily rely on Mo. Here, we review existing studies on alternative nitrogenases in terrestrial settings, spanning inland forests to coastal ecosystems. These studies show frequent Mo limitation of BNF, ubiquitous distribution of alternative nitrogenase genes and significant contributions of alternative nitrogenases to N2 fixation in ecosystems ranging from the tropics to the subarctic. The effect of temperature on nitrogenase isoform activity and regulation is also discussed. We present recently developed methods for measuring alternative nitrogenase activity in the field and discuss the associated analytical challenges. Finally, we discuss how the enzymatic diversity of nitrogenase forces a re-examination of existing knowledge gaps and our understanding of BNF in nature.

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Funding

Funding was provided by Natural Sciences and Engineering Research Council of Canada (Grant No. CRC-950-230570), the U.S. National Science Foundation (Grant No. EAR-1631814), and a Simons Foundation/Life Science Research Foundation Postdoctoral Fellowship (to R.D.).

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  1. Centre Seve, Department of Chemistry, Universite de Sherbrooke, Sherbrooke, QC, Canada

    J. P. Bellenger

  2. Department of Geosciences, Princeton University, Princeton, NJ, USA

    R. Darnajoux & X. Zhang

  3. Princeton Environmental Institute, Princeton University, Princeton, NJ, USA

    X. Zhang & A. M. L. Kraepiel

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  3. X. Zhang
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  4. A. M. L. Kraepiel
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Bellenger, J.P., Darnajoux, R., Zhang, X. et al. Biological nitrogen fixation by alternative nitrogenases in terrestrial ecosystems: a review. Biogeochemistry 149, 53–73 (2020). https://doi.org/10.1007/s10533-020-00666-7

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