The Single-Stranded DNA Genome of Novel Archaeal Virus Halorubrum Pleomorphic Virus 1 Is Enclosed in the Envelope Decorated with Glycoprotein Spikes

Abstract

Only a few archaeal viruses have been subjected to detailed structural analyses. Major obstacles have been the extreme conditions such as high salinity or temperature needed for the propagation of these viruses. In addition, unusual morphotypes of many archaeal viruses have made it difficult to obtain further information on virion architectures. We used controlled virion dissociation to reveal the structural organization of Halorubrum pleomorphic virus 1 (HRPV-1) infecting an extremely halophilic archaeal host. The singlestranded DNA genome is enclosed in a pleomorphic membrane vesicle without detected nucleoproteins. VP4, the larger major structural protein of HRPV-1, forms glycosylated spikes on the virion surface and VP3, the smaller major structural protein, resides on the inner surface of the membrane vesicle. Together, these proteins organize the structure of the membrane vesicle. Quantitative lipid comparison of HRPV-1 and its host Halorubrum sp. revealed that HRPV-1 acquires lipids nonselectively from the host cell membrane, which is typical of pleomorphic enveloped viruses.

Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae

“…The same is true for SH1, where glycolipids, which constitute approximately 20 % of the total host lipids, failed to be detected in viral lipid extracts [7]. Selective incorporation of lipids has been shown for other non-tailed, membrane-containing icosahedral viruses [8,9,30,31], whereas the lipid composition of archaeal and bacterial pleomorphic viruses reflects the host lipid composition [4,41]. Three of the 10 identified structural proteins of P23-77 have been shown to be associated with the capsid, and five with the membrane, while the remaining two could not be unambiguously located [21].…”

Virion Architecture Unifies Globally Distributed Pleolipoviruses Infecting Halophilic Archaea

“…HRPV-1 and HHPV-1 are composed of a membrane vesicle containing two major structural proteins (48,49,53). Although HRPV-1 and HHPV-1 have different genome types (ssDNA versus dsDNA), their circular genomes share the same gene order, and they have homologous structural proteins (49,53).…”

“…The nine (HRPV-1) and eight (HHPV-1) open reading frames (ORF) encode a putative replication initiation protein; two major structural proteins, VP3 and VP4 (VP for virion protein); and a postulated ATPase (HRPV-1 VP8) (49,53). Biochemical analyses of HRPV-1 have shown that VP4 is a spike protein anchored to the membrane and that VP3 is a membrane protein facing the particle interior where the genome resides, without associated nucleoproteins (48). The genome synteny of HRPV-1 and HHPV-1 (from the VP4-encoding gene to the ATPase-encoding gene) is also shared with the linear genome of the haloarchaeal virus His2, which was proposed previously to be spindle shaped (11,49,53).…”

“…Structural studies of icosahedrally symmetric viruses infecting hosts from different domains of life have shown that they are related, and a large number of them can be classified into four structure-based viral lineages (2,3,8,9,13,39). Similarities between HRPV-1 and the bacterial virus L172, which infects Acholeplasma laidlawii, have also led to the proposal of a viral lineage containing pleomorphic viruses from bacteria and archaea (48,49).…”

New, Closely Related Haloarchaeal Viral Elements with Different Nucleic Acid Types

“…It infects Halorubrum sp. and has a pleomorphic appearance with glycosylated spike structures protruding from its external membrane (49,50).…”