Archaeal Host Cell Recognition and Viral Binding of HFTV1 to Its Haloferax Host.

Abstract

Viruses are highly abundant and the main predator of microorganisms. Microorganisms of each domain of life are infected by dedicated viruses. Viruses infecting archaea are genomically and structurally highly diverse. Archaea are undersampled for viruses in comparison with bacteria and eukaryotes. Consequently, the infection mechanisms of archaeal viruses are largely unknown, and most available knowledge stems from viruses infecting a select group of archaea, such as crenarchaea. We employed Haloferax tailed virus 1 (HFTV1) and its host, Haloferax gibbonsii LR2-5, to study viral infection in euryarchaea. We found that HFTV1, which has a siphovirus morphology, is virulent, and interestingly, viral particles adsorb to their host several orders of magnitude faster than most studied haloarchaeal viruses. As the binding site for infection, HFTV1 uses the cell wall component surface (S)-layer protein. Electron microscopy of infected cells revealed that viral particles often made direct contact with their heads to the cell surface, whereby the virion tails were perpendicular to the surface. This seemingly unfavorable orientation for genome delivery might represent a first reversible contact between virus and cell and could enhance viral adsorption rates. In a next irreversible step, the virion tail is orientated toward the cell surface for genome delivery. With these findings, we uncover parallels between entry mechanisms of archaeal viruses and those of bacterial jumbo phages and bacterial gene transfer agents. IMPORTANCE Archaeal viruses are the most enigmatic members of the virosphere. These viruses infect ubiquitous archaea and display an unusually high structural and genetic diversity. Unraveling their mechanisms of infection will shed light on the question if entry and egress mechanisms are highly conserved between viruses infecting a single domain of life or if these mechanisms are dependent on the morphology of the virus and the growth conditions of the host. We studied the entry mechanism of the tailed archaeal virus HFTV1. This showed that despite "typical" siphovirus morphology, the infection mechanism is different from standard laboratory models of tailed phages. We observed that particles bound first with their head to the host cell envelope, and, as such, we discovered parallels between archaeal viruses and nonmodel bacteriophages. This work contributes to a better understanding of entry mechanisms of archaeal viruses and a more complete view of microbial viruses in general.