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Jakub Barylski, Andrew M. Kropinski, Nabil-Fareed Alikhan, Evelien M. Adriaenssens
A summary of this ICTV Report chapter has been published as an ICTV Virus Taxonomy Profile article in the Journal of General Virology, and should be cited when referencing this online chapter as follows:
Jakub Barylski, Andrew M. Kropinski, Nabil-Fareed Alikhan, Evelien M. Adriaenssens and ICTV Report Consortium. 2020, ICTV Virus Taxonomy Profile: Herelleviridae, Journal of General Virology, (In Press)
Members of the family Herelleviridae are bacterial viruses infecting members of the phylum Firmicutes. In the ninth report of the ICTV, this group was reported as the genus SPO1-like viruses. The virions have myovirus morphology, i.e., a head-tail structure with a long, contractile tail, and an icosahedral head. Genomes are dsDNA of 125–170 kb.
Table 1.Herelleviridae. Characteristics of members of the family Herelleviridae
Bacillus phage SPO1 (FJ230960.1), species Bacillus virus SPO1 genus Okubovirus
Head-tail morphology with contractile tail, heads generally isometric with diameters of 85–100 nm showing capsomers, uncontracted tails of 130–185 nm in length
Linear, terminally redundant, non-permuted dsDNA of 125–170 kbp
Phage-encoded DNA polymerase
Bacteria of the phylum Firmicutes
Order Caudovirales, 5 subfamilies, 15 genera and 72 species
Virions have isometric, icosahedral heads of 85–100 nm in diameter. The heads show clear capsomers, i.e. the subunits of the capsid are arranged in pentons and hexons that are assembled into the isometric, icosahedral capsid. The uncontracted tails are 130–185 nm in length. The tails have a baseplate of approximately 60 nm and a small collar (Table 1.Herelleviridae, Figure 1.Herelleviridae).
Figure 1.Herelleviridae. Transmission electron micrograph of Bacillus phage phiAGATE, a member of the family Herelleviridae (subfamily Bastillevirinae). Virions were concentrated from bacteria-free lysates and stained with 2% uranyl acetate. Negatively-stained phage particles were visualized using a JEOL JEM-1400 transmission electron microscope at 120 kV.
Bacillus phage SPO1 buoyant density in CsCl is 1.54 g/cm3.
The genomes of herelleviruses consist of linear dsDNA with long terminal repeats of 3–16 kbp (Perkus and Shub 1985, Klumpp et al., 2008, Łobocka and Szybalski 2012). Genomes are of 125–170 kbp. tRNAs are encoded by some members. The genome of Bacillus phage SPO1 has thymidine replaced with 5-hydroxymethyluridine and this modification or a similar one could be present in all members of the family (Okubo et al., 1972, Parker and Eiserling 1983, Klumpp et al., 2010).
The virion of Bacillus phage SPO1 comprises at least 35 proteins as judged from electropherograms of purified particles (Parker and Eiserling 1983).
No lipids reported.
No carbohydrates reported.
The genomes of herelleviruses are linear dsDNA with long terminal repeats of various lengths. Genomes are of 125–170 kbp and encode 165–301 genes, including 0–24 tRNAs. For Bacillus phage SPO1, the majority of the coding sequences are in the same orientation; two islands encoding hypothetical proteins are transcribed from the opposite strand (Figure 2.Herelleviridae). The terminal repeat of SPO1 contain a host-takeover module involved in phage propagation. Transcription is mediated by phage-encoded sigma factors that co-opt the host RNA polymerase (Stewart et al., 2009). Introns have been identified in a number of herellevirus genomes (Goodrich-Blair et al., 1990, Lavigne and Vandersteegen 2013).
Figure 2.Herelleviridae. Genome organisation of Bacillus phage SPO1, the typical member of the family Herelleviridae. The terminal repeat area is indicated with a blue arc, structural modules with a cyan arcs. The predicted coding sequences on the plus-strand are in purple, those on the minus-strand in teal. The five predicted tRNAs are indicated in black. This figure was generated with BRIG (Alikhan et al., 2011).
Table 2.Herelleviridae. Core genes with predicted functions shared among all members of the family*
Prokaryotic virus orthologous group number
baseplate J-like protein
tail sheath protein
terminase large subunit (intron-invaded)
major capsid protein
DNA polymerase I
tail tape measure protein
tail tube protein
The phages belonging to this family are reported to be obligately lytic, but some may be able to cause persistent infection, pseudolysogenic infection or a carrier state (Schuch and Fischetti 2009, Yuan et al., 2015). Herelleviruses infect bacteria belonging to the phylum Firmicutes and have a worldwide distribution.
Subfamilies (Table 3.Herelleviridae) are identified as well-supported monophyletic groups based on phylogenetic analysis of concatenated core gene markers and single core genes (Figure 3.Herelleviridae). Within a subfamily, members are 20–25% identical in translated nucleotide content as calculated with the tBLASTx algorithm. Between members of different subfamilies, there is little to no nucleotide sequence identity across the genome length.
Table 3.Herelleviridae. The subfamilies of Herelleviridae
Staphylococcus and Lactobacillus
The Herelleviridae genera are well-supported monophyletic clades in genome-based phylogenies and in (concatenated) marker gene phylogenies. Members of the genus share at least 60% nucleotide identity across the genome length. The genome organisation is conserved. Members of the same genus generally infect members of the same bacterial genus.
The species demarcation criteria are the same for all species within this family. Members of the same species are more than 95% identical in genome nucleotide sequence, including the terminal repeat region. Phages with genomes that differ in more than 5% are assigned to different species.
Herelleviridae – named in honour of the 100th anniversary of the discovery of bacteriophages by Félix d’Hérelle in 1917.
Phylogenetic analysis of 10 core gene products shared among all herelleviruses (Barylski et al., 2019) has identified five subfamilies, 15 genera and 72 species, of which seven species do not belong to a genus and three species do not belong to a genus or subfamily. (Figure 3.Herelleviridae). The relationships are largely conserved in single marker gene phylogenies, however, shuffling between subfamilies has been observed for the tail tube protein (Barylski et al., 2019).
Figure 3.Herelleviridae. Phylogenetic analysis of members of the family Herelleviridae. Amino acid sequences of 10 concatenated core proteins as identified in (Barylski et al., 2019) were aligned with Clustal Omega. A mid-point rooted maximum likelihood tree was generated with the IQ-TREE pipeline including ModelFinder on a partitioned model of the alignment. Ultrafast boostraps (UFBOOT) scores out of 100 indicate branch support. The scale bar represents the number of substitutions per site. Open circles indicate viruses classified to a species but not to a genus.
Herelleviruses share morphological similarity with other myoviruses, i.e. bacteriophages with long contractile tails.
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