Particle Assembly and Ultrastructural Features Associated with Replication of the Lytic Archaeal Virus Sulfolobus Turreted Icosahedral Virus

Abstract

Little is known about the replication cycle of archaeal viruses. We have investigated the ultrastructural changes of Sulfolobus solfataricus P2 associated with infection by Sulfolobus turreted icosahedral virus (STIV). A time course of a near synchronous STIV infection was analyzed using both scanning and transmission electron microscopy. Assembly of STIV particles, including particles lacking DNA, was observed within cells, and fully assembled STIV particles were visible by 30 h postinfection (hpi). STIV was determined to be a lytic virus, causing cell disruption beginning at 30 hpi. Prior to cell lysis, virus infection resulted in the formation of pyramid-like projections from the cell surface. These projections, which have not been documented in any other host-virus system, appeared to be caused by the protrusion of the cell membrane beyond the bordering S-layer. These structures are thought to be sites at which progeny virus particles are released from infected cells. Based on these observations of lysis, a plaque assay was developed for STIV. From these studies we propose an overall assembly model for STIV.

Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome

“…Not only the morphotypes but also the genomes of hyperthermophilic archaeal viruses are exceptional: more than 90% of their putative genes have no recognizable functions or detectable homologs in other viruses or cellular life forms (6,10,11). Moreover, the ways in which some of these viruses interact with their hosts are also particular, as recently demonstrated by the description of a unique virion release mechanism (12)(13)(14).…”

Structure and assembly mechanism of virus-associated pyramids

“…Virus-associated pyramids are the central feature of the egress mechanism of at least two archaeal viruses: SIRV2 and STIV1 (Bize et al 2009;Brumfield et al 2009). SIRV2 is member of the family Rudiviridae and its linear double-stranded (ds)DNA genome is wrapped in a rod-shaped capsid of9 00 nm in length and 23 nm in diameter (Zillig et al 1993;Prangishvili et al 1999;Peng et al 2001;DiMaio et al 2015).…”

“…An especially striking example is the virion release (egress) mechanism shared by the STIV1 (Sulfolobus turreted icosahedral virus 1) and SIRV2 (Sulfolobus islandicus rod-shaped virus 2). Both viruses infect members of the hyperthermophilic order Sulfolobales that grow optimally in hot acidic environments (~75°C, pH 3) (Bize et al 2009;Brumfield et al 2009), are lytic and are released from the cell via remarkable pyramidal egress structures that allow the formation of defined apertures in the cell membrane (Bize et al 2009;Brumfield et al 2009;Prangishvili and Quax 2011). These virus-associated pyramids (VAPs) display sevenfold symmetry and form stable assemblies that can be isolated from the cell .…”

Archaeal viruses—novel, diverse and enigmatic

“…The product is an empty, thick-shelled, rounded particle, with a circular inner membrane, devoid of nucleic acid ( Figure 6). After packaging of the genome, possibly employing a similar mechanism to bacteriophage PRD1, particles appear more angular with thinner shells characteristic of mature particles ( Figure 6) [42]. Simultaneously, pyramidal structures form on the cell surface, in regions devoid of S-layer proteins, through which the virions were inferred to extrude from the cells (Figure 6) [42].…”

“…The first attempts to view virion assembly in vivo were performed on the turreted icosahedral lytic virus STIV1 using electron microscopy [42]. In near synchronously infected cells, mature virions appeared about 24 h p.i, together with immature virus particles lacking dense cores.…”