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  1. Mapping the structural dynamics of the DNA gyrase N-gate

    Parente, Angelica Coco
    [Stanford, California] : [Stanford University], 2018.

    DNA gyrase is an essential bacterial molecular motor that uses ATP hydrolysis to drive the directional introduction of DNA supercoils. The enzyme employs a duplex strand passage mechanism that requires coordinating the opening and closing of three protein "gates": the N-gate, DNA-gate, and Exit-gate. The N-gate is formed by the dimerization of ATPase domains and acts as a nucleotide-dependent clamp that captures DNA for subsequent strand passage. Dynamic measurements of N-gate conformational changes are necessary to understand how gyrase harnesses chemical energy to direct changes in DNA topology. Here, we report real-time single molecule measurements of E. coli gyrase N-gate conformational dynamics under varying DNA and nucleotide conditions. We identify a landscape of distinct conformational intermediates whose populations can be shifted upon DNA and nucleotide binding. The N-gate is primarily open in the absence of DNA and nucleotide, but transiently samples closed conformations. The non-hydrolyzable ATP analog AMPPNP, but not ADP, induces stable N-gate dimerization, where FRET values are consistent with a closed conformation seen in crystal structures based on in silico modeling of dye positions. In the presence of DNA, the enzyme samples a distinct high FRET conformation of the N-gate that is consistent with an intermediate conformation previously described in studies of B. subtilis gyrase. Our measurements support a loose-coupling model in which N-gate conformations are highly dynamic and depend on both DNA and nucleotide binding. Substrate-induced N-gate conformational changes appear to be conserved across divergent bacterial species and could extend to other enzymes in the Gyrase-Hsp90-MutL (GHL) ATPase family. This work sets the stage for detailed structural modeling and for multimodal measurements that directly correlate protein and DNA dynamics in this complex molecular machine.

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