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

Abstract

A new family of viruses named Sphaerolipoviridae has been proposed recently. It comprises icosahedral, tailless haloarchaeal viruses with an internal lipid membrane located between the protein capsid and the dsDNA genome. The proposed family Sphaerolipoviridae was divided into two genera: Alphasphaerolipovirus, including Haloarcula hispanica viruses SH1, PH1 and HHIV-2, and Betasphaerolipovirus, including Natrinema virus SNJ1. Here, we propose to expand the family Sphaerolipoviridae to include a group of bacteriophages infecting extreme thermophilic Thermus thermophilus and sharing a number of structural and genomic properties with archaeal sphaerolipoviruses. This new group comprises two members, lytic phage P23-77 and temperate phage IN93, as well as putative members P23-72 and P23-65H. In addition, several related proviruses have been discovered as integrated elements in bacterial genomes of the families Thermus and Meiothermus. Morphology of the virus particles and the overall capsid architecture of these bacteriophages resembles that of archaeal members of the Sphaerolipoviridae, including an unusual capsid arrangement in a T = 28 dextro lattice. Alpha-and betasphaerolipoviruses share with P23-77-like bacteriophages a conserved block of core genes that encode a putative genome-packaging ATPase and the two major capsid proteins (MCPs). The recently determined X-ray structure of the small and large MCPs of P23-77 revealed a single beta-barrel (jelly-roll) fold that is superimposable with the cryo-EM density maps of the SH1 capsomers. Given the common features of these viruses, we propose to include the so far unclassified P23-77-like bacteriophages into a new genus, ''Gammasphaerolipovirus'', within the family Sphaerolipoviridae.

Sulfolobus Spindle-Shaped Virus 1 Contains Glycosylated Capsid Proteins, a Cellular Chromatin Protein, and Host-Derived Lipids

“…Moreover, in-frame deletion of the VP2-encoding gene had no observable effect on virion assembly or infectivity, indicating that the gene is dispensable under laboratory growth conditions (79). Interestingly, unlike other SSV1 VPs, VP2 is not specific to fuselloviruses but also is encoded by unrelated proviruses of the euryarchaeon Archaeoglobus veneficus SNP6 (80), Sulfolobus turreted icosahedral virus 2 (81), and bacterial viruses of the recently established family Sphaerolipoviridae (82). Such patchy phyletic distribution of vp2-like genes in fuselloviruses, its conservation in other archaeal and bacterial viruses, and the dispensability of VP2 for SSV1 infectivity indicate that the vp2 gene has been acquired relatively late in the history of fuselloviruses from a different group of viruses.…”

The Minor Capsid Protein VP11 of Thermophilic Bacteriophage P23-77 Facilitates Virus Assembly by Using Lipid-Protein Interactions

“…Initial studies have shown that the VP11-encoding gene (ORF11) is exclusively found in P23-77 and has no homologs in the related sphaerolipovirus IN93 or associated proviruses (4,34,35). The only similarity we detected in data bank searches was to a protein sequence derived from Meiothermus timidus, indicating the presence of a P23-77-like provirus.…”

“…With respect to extreme thermophilic bacteria, the virus studied best on the structural level is P23-77, a strictly lytic phage infecting Thermus thermophilus ATCC 33923 (1,2,3). P23-77 is a representative of the novel Sphaerolipoviridae, comprising viruses infecting members of two domains of life, namely, extreme halophilic archaea of the family Halobacteriaceae and thermophilic bacteria of the family Thermaceae (4). All the family members have similar virion morphologies.…”

“…The only similarity we detected in data bank searches was to a protein sequence derived from Meiothermus timidus, indicating the presence of a P23-77-like provirus. ORF11 is located in the genome in an area with variable gene content, which comprises genes with predicted function in DNA packaging and virus exit (4,34) (Fig. 1A).…”

A virus of hyperthermophilic archaea with a unique architecture among DNA viruses

“…However, some of these minor proteins might form terminal filaments of PFV1. Examples of interchangeable gene cassettes encoding receptor-binding proteins are known from several different families of archaeal viruses, including Lipothrixviridae, Sphaerolipoviridae, and Fuselloviridae (37)(38)(39)(40). Most of the minor structural proteins of PFV1 are encoded in the vicinity of the three major virion proteins (Fig.…”