Herelleviridae


Herelleviridae

Jakub Barylski, Andrew M. Kropinski, Nabil-Fareed Alikhan, Evelien M. Adriaenssens

Chapter contents

Posted January 2020

Herelleviridae: The family

Member taxa

Supporting information

  • Authors - corresponding author: Evelien M Adriaenssens (evelien.adriaenssens@quadram.ac.uk)
  • Resources - web resources, sequence alignments and tree files
  • Further reading - reviews and additional information
  • References

Citation 

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: HerelleviridaeJournal of General Virology, (In Press)

Summary 

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

Characteristic

Description

Typical member

Bacillus phage SPO1 (FJ230960.1), species Bacillus virus SPO1 genus Okubovirus

Virion

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

Genome

Linear, terminally redundant, non-permuted dsDNA of 125–170 kbp

Replication

Phage-encoded DNA polymerase

Translation

Bacterial translation

Host range

Bacteria of the phylum Firmicutes

Taxonomy

Order Caudovirales, 5 subfamilies, 15 genera and 72 species

Virion 

Morphology

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. 

Physicochemical and physical properties      

Bacillus phage SPO1 buoyant density in CsCl is 1.54 g/cm3.

Nucleic acid

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).

Proteins

The virion of Bacillus phage SPO1 comprises at least 35 proteins as judged from electropherograms of purified particles (Parker and Eiserling 1983).

Lipids

No lipids reported.

Carbohydrates

No carbohydrates reported.

Genome organization and replication

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*

Gene

Prokaryotic virus orthologous group number

DnaB-like helicase

VOG0025, VOG4691

baseplate J-like protein

VOG4644

tail sheath protein

VOG0067

terminase large subunit (intron-invaded)

VOG0051

major capsid protein

VOG0061

prohead protease

VOG4568

portal protein

VOG4556

DNA primase

VOG4551

DNA polymerase I

VOG0668

RNA polymerase

VOG0118

recombination exonuclease

VOG4575

recombination endonuclease

VOG0083

tail tape measure protein

VOG0069

tail tube protein

VOG0068

* at a 50% amino acid sequence identity threshold at minimum 50% gene coverage or by prokaryotic Virus Orthologous Group (pVOG) analysis (Barylski et al., 2019

Biology

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. 

Subfamily demarcation criteria 

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

Subfamily

Genera

Host

Genome (kbp)

Terminal repeats*

Bastillevirinae

7

Bacillus sp.

146167

Long

Brockvirinae

1

Enterococcus sp.

140–155

ND

Jasinkavirinae

1

Listeria monocytogenes

131–138

ND

Spounavirinae

2

Bacillus sp.

132–146

Long

Twortvirinae

4

Staphylococcus and Lactobacillus

135–150

ND

*ND Not Determined for all members

Genus demarcation criteria

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.

Species demarcation criteria

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. 

Derivation of names 

Herelleviridae – named in honour of the 100th anniversary of the discovery of bacteriophages by Félix d’Hérelle in 1917.

Phylogenetic relationships

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. This phylogenetic tree and corresponding sequence alignment are available to download from the Resources page.

Similarity with other taxa 

Herelleviruses share morphological similarity with other myoviruses, i.e. bacteriophages with long contractile tails.

Species unassigned to a subfamily

Exemplar isolate of the species
SpeciesVirus nameIsolateAccession numberRefSeq numberAvailable sequenceVirus Abbrev.
Brochothrix virus A9Brochothrix phage A9HM242243NC_015253Complete genome
Lactobacillus virus Lb338-1Lactobacillus phage Lb338-1FJ822135NC_012530Complete genome
Lactobacillus virus LP65Lactobacillus phage LP65AY682195NC_006565Complete genome

Virus names, the choice of exemplar isolates, and virus abbreviations, are not official ICTV designations.