His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus

Abstract

Spindle-shaped viruses are a dominant morphotype in hypersaline waters but their molecular characteristics and their relationship to other archaeal viruses have not been determined. Here, we describe the isolation, characteristics and genome sequence of His2, a spindle-shaped halovirus, and compare it to the previously reported halovirus His1. Their particle dimensions, host-ranges and buoyant densities were found to be similar but they differed in their stabilities to raised temperature, low salinity and chloroform. The genomes of both viruses were linear dsDNA, of similar size (His1, 14,464 bp; His2, 16,067 bp) and mol% G+C (approximately 40%), with long, inverted terminal repeat sequences. The genomic termini of both viruses are likely to possess bound proteins. They shared little nucleotide similarity and, except for their putative DNA polymerase ORFs, no significant similarity at the predicted protein level. A few of the 35 predicted ORFs of both viruses showed significant matches to sequences in GenBank, and these were always to proteins of haloarchaea. Their DNA polymerases showed 42% aa identity, and belonged to the type B group of replicases that use protein-priming. Purified His2 particles were composed of four main proteins (62, 36, 28 and 21 kDa) and the gene for the major capsid protein was identified. Hypothetical proteins similar to His2 VP1 are present in four haloarchaeal genomes but are not part of complete prophages. This, and other evidence, suggests a high frequency of recombination between haloviruses and their hosts. His1 and His2 are unlike fuselloviruses and have been placed in a new virus group, Salterprovirus.

Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere

“…Viruses with a spindle-shaped appearance have been isolated from hyperthermophilic and halophilic euryarchaeal hosts of the orders Thermococcales (Pyrococcus abyssi virus 1 [PAV1]) and Halobacteriales (viruses His1 and His2), respectively (15,91). Similarly to crenarchaeal fuselloviruses (231), these viruses display plasticity in virion morphology, which ranges from spindle shaped to elongated and flattened (for PAV1 [91]) or oblate and pleomorphic (for His2 [15]). Similarly, preparations of the predominantly pleomorphic haloarchaeal virus Haloarcula hispanica pleomorphic virus 1 (HHPV-1) occasionally also contain spindle-shaped particles (236).…”

“…Both viruses encode type B DNA polymerases, and their genomes are likely to be replicated in a protein-primed manner (15,210). The two viruses are only distantly related to each other, with generally no similarity between their corresponding protein sequences (15).…”

“…8). The other module encodes proteins implicated in His2 genome replication (DNA polymerase and a number of proteins with potential zinc finger DNA-binding motifs [15]). Such a module is not present in the circular HHPV-1 genome, which instead encodes a putative rolling-circle replication (RCR) initiation protein at an equivalent Fig.…”

Archaeal Extrachromosomal Genetic Elements

“…The vast majority of reported archaeal viruses contain a dsDNA genome, and most of the dsDNA genomes are circular or linear, with covalently closed ends. Linear dsDNA genomes with ends covalently linked to a protein have also been found (23,86,87). Only five archaeal viruses (i.e., ACV, HRPV1/2/6, and HHPV2) are currently known to carry an ssDNA genome.…”

Phage φ29 and Nf terminal protein-priming domain specifies the internal template nucleotide to initiate DNA replication

“…M any organisms, such as bacteriophages; animal viruses, such as adenovirus, mitochondrial plasmids, linear chromosomes and plasmids of Streptomyces (1); and more recently virus infecting Archaea, such as halovirus (2,3), possess replication origins constituted by inverted terminal repetitions (ITR) with a terminal protein (TP) linked to both 5Ј ends of their linear chromosomes (4). In these cases, the location of the 2 replication origins allows both strands to be replicated continuously, without requiring asymmetric complexes of DNA polymerase with other accessory proteins to control the different mechanics of continuous and discontinuous DNA synthesis (5).…”