A Touch of Sleep: Biophysical Model of Contact-mediated Dormancy of Archaea by Viruses

Abstract: The canonical view of the interactions between viruses and their microbial hosts presumes that changes in host and virus fate require the initiation of infection of a host by a virus. That is, first virus particles diffuse randomly outside of host cells, then the virus genome enters the target host cell, and only then do intracellular dynamics and regulation of virus and host cell fate unfold. Intracellular dynamics may lead to the death of the host cell and release of viruses, to the elimination of the virus genome through cellular defense mechanisms, or the integration of the virus genome with the host as a chromosomal or extra-chromosomal element. Here we revisit this canonical view, inspired by recent experimental findings of Bautista and colleagues (mBio, 2015) in which the majority of target host cells can be induced into a dormant state when exposed to either active or de-activated viruses, even when viruses are present at low relative titer. We propose that both the qualitative phenomena and the quantitative time-scales of dormancy induction can be reconciled given the hypothesis that cellular physiology can be altered by contact on the surface of host cells rather than strictly by infection. We develop a biophysical model of contact-mediated dynamics involving virus particles and target cells. We show how in this model virus particles can catalyze - extracellularly - cellular transformations amongst many cells, even if they ultimately infect only one (or none). We discuss implications of the present biophysical model relevant to the study of virus-microbe interactions more generally.