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Reconstructed ancient nitrogenases suggest Mo-specific ancestry

View ORCID ProfileAmanda K. Garcia, View ORCID ProfileHanon McShea, View ORCID ProfileBryan Kolaczkowski, View ORCID ProfileBetül Kaçar
doi: https://doi.org/10.1101/714469
Amanda K. Garcia
1Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona
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Hanon McShea
2Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts
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Bryan Kolaczkowski
3Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida
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Betül Kaçar
1Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona
4Department of Astronomy and Steward Observatory, University of Arizona, Tucson, Arizona
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  • For correspondence: betul@arizona.edu
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ABSTRACT

The nitrogenase metalloenzyme family, essential for supplying fixed nitrogen to the biosphere, is one of life’s key biogeochemical innovations. The three isozymes of nitrogenase differ in their metal dependence, each binding either a FeMo-, FeV-, or FeFe-cofactor for the reduction of nitrogen. The history of nitrogenase metal dependence has been of particular interest due to the possible implication that ancient marine metal availabilities have significantly constrained nitrogenase evolution over geologic time. Here, we combine phylogenetics and ancestral sequence reconstruction — a method by which inferred, historical protein sequence information can be linked to functional molecular properties — to reconstruct the metal dependence of ancient nitrogenases. Inferred ancestral nitrogenase sequences at the deepest nodes of the phylogeny suggest that ancient nitrogenases were Mo-dependent. We find that active-site sequence identity can reliably distinguish extant Mo-nitrogenases from V- and Fe-nitrogenases, as opposed to modeled active-site structural features that cannot be used to reliably classify nitrogenases of unknown metal dependence. Taxa represented by early-branching nitrogenase lineages lack one or more biosynthetic nifE and nifN genes that are necessary for assembly of the FeMo-cofactor, suggesting that early Mo-dependent nitrogenases may have utilized an alternate pathway for Mo- usage predating the FeMo-cofactor. Our results underscore the profound impacts that protein-level innovations likely had on shaping global biogeochemical cycles throughout Precambrian, in contrast to organism-level innovations which characterize Phanerozoic eon.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 25, 2019.
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Reconstructed ancient nitrogenases suggest Mo-specific ancestry
Amanda K. Garcia, Hanon McShea, Bryan Kolaczkowski, Betül Kaçar
bioRxiv 714469; doi: https://doi.org/10.1101/714469
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Reconstructed ancient nitrogenases suggest Mo-specific ancestry
Amanda K. Garcia, Hanon McShea, Bryan Kolaczkowski, Betül Kaçar
bioRxiv 714469; doi: https://doi.org/10.1101/714469

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