Coupling of the hydration shell of B-DNA to conformational substates and peptide recognition studied by time-resolved FTIR spectroscopy


Coupling of the hydration shell of B-DNA to conformational substates and peptide recognition studied by time-resolved FTIR spectroscopy

Khesbak, H.; Savchuk, O.; Tsushima, S.; Fahmy, K.

Biomolecular recognition typically proceeds in an aqueous environment, where hydration shells are a constitutive part of the interacting species. The coupling of hydration shell structure to conformation is particularly pronounced for DNA with its large surface to volume ratio. Conformational substates of the phosphodiester backbone in B-DNA contribute to DNA flexibility and are strongly dependent on hydration. We have studied by rapid scan FTIR spectroscopy the isothermal BI-BII transition on its intrinsic time scale of seconds. Correlation analysis of IR absorption changes induced by an incremental growth of the DNA hydration shell identifies water populations w1 (PO2--bound) and w2 (non-PO2--bound) exhibiting weaker and stronger H-bonds, respectively, than those in bulk water. The BII substate is stabilized by w2. The water H-bond imbalance of 3-4 kJ mol-1 is equalized at little enthalpic cost upon formation of a contiguous water network (at 12-14 H2O molecules per DNA phosphate) of reduced (OH) band width. In this state, hydration water cooperatively stabilizes the BI conformer via the entropically favored replacement of w2-DNA interactions by additional w2-water contacts, rather than binding to BI-specific hydration sites. Such water rearrangements contribute to the recognition of DNA by indolicidin, an antimicrobial 13-mer peptide from bovine neutrophils which, despite little intrinsic structure, preferentially binds to the BI conformer in a water-mediated induced fit. In combination with CD-spectral titrations, the data indicate that in the absence of a bulk aqueous phase, as in molecular crowded environments, water relocation within the DNA hydration shell allows for entropic contributions similar to those assigned to water upon DNA ligand recognition in solution.

Keywords: infrared spectroscopy; molecular recognition; DNA structure

  • Contribution to proceedings
    8th European Biophysics Congress, 23.-27.08.2011, Budapest, Hungary
    European Biophysics Journal with Biophysics Letters 40 (2011), 45

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Publ.-Id: 15697