Molecular mechanisms underlying the thermal response of cells remain elusive. On the basis of the recent result that the short-time diffusive dynamics of the Escherichia coli proteome is an excellent indicator of temperature-dependent bacterial metabolism and death, we used neutron scattering (NS) spectroscopy and molecular dynamics (MD) simulations to investigate the sub-nanosecond proteome mobility in psychro-, meso-, and hyperthermophilic bacteria over a wide temperature range. The magnitude of thermal fluctuations, measured by atomic mean square displacements, is similar among all studied bacteria at their respective thermal cell death. Global roto-translational motions turn out to be the main factor distinguishing the bacterial dynamical properties. We ascribe this behavior to the difference in the average proteome net charge, which becomes less negative for increasing bacterial thermal stability. We propose that the chemical-physical properties of the cytoplasm and the global dynamics of the resulting proteome are fine-tuned by evolution to uphold optimal thermal stability conditions.

Department of Physics and Geology University of Perugia Via Alessandro Pascoli 06123 Perugia Italy

Institut de Biologie Physico Chimique Fondation Edmond de Rothschild 13 Rue Pierre et Marie Curie 75005 Paris France

Institut Laue Langevin 71 Avenue des Martyrs CS 20156 38042 Grenoble France

Institut Universitaire de France 75231 Paris France

J Heyrovský Institute of Physical Chemistry Czech Academy of Sciences 182 23 Prague Czech Republic

Laboratoire de Biochimie Théorique Université de Paris Cité 75005 Paris France

Laboratoire de Bioénergétique et Ingénierie des Protéines Aix Marseille Université 13400 Marseille France

Laboratoire Interdisciplinaire de Physique Centre National de la Recherche Scientifique Univ Grenoble Alpes 140 Rue de la Physique 38402 Saint Martin d'Hères France

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Diffusive Dynamics of Bacterial Proteome as a Proxy of Cell Death