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Anticipatory active-site motions and chromophore distortion prime photoreceptor PYP for light activation

Nature Structural & Molecular Biology volume 10, pages 663–668 (2003)Cite this article

Abstract

Protein photoreceptors use small-molecule cofactors called chromophores to detect light. Only under the influence of the receptors' active sites do these chromophores adopt spectral and photochemical properties that suit the receptors' functional requirements. This protein-induced change in chromophore properties is called photochemical tuning and is a prime example for the general—but poorly understood—process of chemical tuning through which proteins shape the reactivity of their active-site groups. Here we report the 0.82-Å resolution X-ray structure of the bacterial light receptor photoactive yellow protein (PYP). The unusually precise structure reveals deviations from expected molecular geometries and anisotropic atomic displacements in the PYP active site. Our analysis of these deviations points directly to the intramolecular forces and active-site dynamics that tune the properties of PYP's chromophore to absorb blue light, suppress fluorescence, and favor the required light-driven double-bond isomerization.

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Figure 1: Chromophore electronic state derived from experimentally determined bonding distances.
Figure 2: Relationship between chromophore bowing and fluorescence.
Figure 3: Conformational plasticity in PYP active site.
Figure 4: Atomic collisions associated with active-site displacement modes.
Figure 5: Coordination of atomic motions in the preferred displacement mode (Fig. 4a).

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Acknowledgements

We thank C. Putnam for generating the photographs in Figure 2 and 1. Canestrelli for growing the crystals used in this study. Portions of this research were carried out at the Stanford Synchrotron Radiation Laboratory (SSRL), a national user facility operated by Stanford University on behalf of the US Department of Energy (DOE), Office of Basic Energy Sciences. The SSRL Structural Molecular Biology Program is supported by the DOE, Office of Biological and Environmental Research, and by the US National Institutes of Health (NIH), US National Center for Research Resources, Biomedical Technology Program and the US National Institute of General Medical Sciences. This work was supported through a vision research grant from the Karl Kirchgessner Foundation (U.K.G.) and a grant from the NIH (E.D.G.).

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Authors and Affiliations

  1. Department of Molecular Biology, The Scripps Research Institute, La Jolla, 92037, California, USA

    Elizabeth D Getzoff & Ulrich K Genick

  2. Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, 92037, California, USA

    Elizabeth D Getzoff

  3. Department of Biochemistry, Brandeis University, Waltham, 02454, Massachusetts, USA

    Karl N Gutwin & Ulrich K Genick

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  1. Elizabeth D Getzoff
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Correspondence to Elizabeth D Getzoff.

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Getzoff, E., Gutwin, K. & Genick, U. Anticipatory active-site motions and chromophore distortion prime photoreceptor PYP for light activation. Nat Struct Mol Biol 10, 663–668 (2003). https://doi.org/10.1038/nsb958

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