Chaseviridae

Chaseviridae

Hany Anany, Padmanabhan Mahadevan, Dann Turner, Evelien M. Adriaenssens, Andrew M. Kropinski

The citation for this ICTV Report chapter is the summary published as Anany et al., (2021):
ICTV Virus Taxonomy Profile: Chaseviridae 2021, Journal of General Virology (in press)

Corresponding author: Hany Anany (hany.anany@agr.gc.ca, hanany@alumni.uoguelph.ca)
Edited by:  Evelien M. Adriaenssens and Stuart G. Siddell
Posted:  November 2021

Summary

Members of the family Chaseviridae are bacterial viruses infecting representatives of the bacterial class Gammaproteobacteria. Virions of members of this family have myovirus morphology, i.e., a head-tail structure with a long, contractile tail, and an icosahedral head (Table 1.Chaseviridae). Genomes are dsDNA of 52–56 kbp with G+C content ranging from 39.3–52.5%.  Chaseviruses, like members of the family Autographiviridae,  encode a large single subunit RNA polymerase, but unlike those viruses their promoter sequences have not yet been identified.

Table 1.Chaseviridae Characteristics of members of the family Chaseviridae

Characteristic

Description

Example

Escherichia phage vB_EcoM-4HA13 (MN136198), species Escherichia virus 4HA13, genus Sabourvirus

Virion

Head-tail morphology with contractile tail; heads generally isometric with diameters of 53–65 nm showing capsomers, uncontracted tails of 116–166 nm in length

Genome

Linear, terminally redundant, non-permuted dsDNA of 52–56 kbp

Replication

Phage-encoded DNA polymerase

Translation

Bacterial translation

Host range

Bacteria of the phylum Proteobacteria, class Gammaproteobacteria

Taxonomy

Realm Duplodnaviria;, kingdom Heunggongvirae, phylum Uroviricota, class Caudoviricetes, order Caudovirales; 2 subfamilies (Nefertitivirinae, Cleopatravirinae), 8 genera and 14 species

Virion

Morphology

Virions have isometric, icosahedral heads of 53–65 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 contracted tails are 116–166 nm in length. (Figure 1.Chaseviridae).

Figure 1.Chaseviridae. Transmission electron micrographs of negatively stained phages. (A) Escherichia phage vB_EcoM-4HA13, (B) Erwinia phage vB_EamM-Y2 (provided by Martin J. Loessner) and (C) Escherichia phage phiEcoM-GJ1 (provided by Nidham Jamalludeen).

Physicochemical and physical properties

Not determined.

Nucleic acid

The genomes of members of the family Chaseviridae consist of linear dsDNA with long terminal repeats of approximately 3 kbp. Genomes range between 52–56 kbp. Some members are predicted to encode tRNAs. There is no report of modified bases in the DNA of these viruses. A genome diagram of Escherichia phage vB_EcoM-4HA13, is typical of the family (Figure 2.Chaseviridae).

Figure 2. Genome organisation of Escherichia phage vB_EcoM-4HA13. Genes involved in transcription are coloured red, DNA and nucleotide synthesis, blue; homing endonucleases, orange; packaging, pink; morphogenesis, green; and lysis brown. The linear genome is represented as a circle with the green arc representing the left LTR. This figure was generated with GenomeVx (Conant and Wolfe 2008) and edited with Foxit PDF Editor.

Proteins

The virion proteins of three members of this family, Escherichia phage phiEcoM-GJ1 (Jamalludeen et al., 2008),  Escherichia phage vB_EcoM-4HA13 and, Erwinia phage vB_EraM-Y2 (Born et al., 2011) have been investigated using mass spectrometry.  In the case of Escherichia phage vB_EcoM-4HA13, 15 structural proteins were identified with the major capsid protein containing an acetylated lysine residue.

Genome organization and replication

The genomes of chaseviruses are linear dsDNA with long terminal repeats of approximately 3 kbp. Genomes are of 52–56 kbp and encode 63–92 genes, including 0–1 tRNAs. For Escherichia phage vB_EcoM-4HA13, all coding sequences are transcribed off a single strand  (Figure 2.Chaseviridae). Transcription is mediated by the host and a phage-encoded Autographiviridae-like RNA polymerase. DNA replication is mediated by a phage-encoded DNA polymerase and DNA helicase/primase.

Comparing all chaseviruses at the protein level, using CoreGenes 5.0 (https://coregenes.ngrok.io/ and by ViPTree analysis (Nishimura et al. 2017)) with the OrthoMCL algorithm (Li et al., 2003), reveals 25 conserved proteins representing 33.7% of the viral proteome. The conserved proteins were identified using PHROGS ((Terzian et al., 2021); https://phrogs.lmge.uca.fr/) and are presented in Table 2.Chaseviridae.

Table 2.Chaseviridae. Core genes (with predicted functions) shared among all members of the family (identified using CoreGenes 5.0 and mapped to the PHROGS database).

NCBI prot ID*

PHROG number

PHROG annotation

PHROG category

YP_001595396.1

phrog_414

RNA polymerase

DNA, RNA and nucleotide metabolism

YP_001595423.1

phrog_13087

unknown function

unknown function

YP_001595430.1

phrog_239

DNA primase/helicase

DNA, RNA and nucleotide metabolism

YP_001595432.1

phrog_17

DNA polymerase

DNA, RNA and nucleotide metabolism

YP_001595434.1

phrog_862

unknown function

unknown function

YP_001595435.1

phrog_107

RNaseH

DNA, RNA and nucleotide metabolism

YP_001595436.1

phrog_1985

HNH endonuclease

DNA, RNA and nucleotide metabolism

YP_001595438.1

phrog_139

deoxynucleoside monophosphate kinase

other (intermediary metabolism)

YP_001595443.1

phrog_38

terminase large subunit

head and packaging

YP_001595445.1

phrog_146

portal protein

head and packaging

YP_001595446.1

phrog_530

head maturation protease

head and packaging

YP_001595447.1

phrog_563

virion structural protein

head and packaging

YP_001595448.1

phrog_264

major head protein

head and packaging

YP_001595450.1

phrog_302

virion structural protein

head and packaging

YP_001595451.1

phrog_11887

head protein

head and packaging

YP_001595452.1

phrog_12771

tail completion

connector

YP_001595453.1

phrog_205

virion structural protein

head and packaging

YP_001595454.1

phrog_280

virion structural protein

head and packaging

YP_001595455.1

phrog_11820

tail assembly chaperone

tail

YP_001595458.1

phrog_196

virion structural protein

head and packaging

YP_001595461.1

phrog_11

baseplate protein

tail

YP_001595462.1

phrog_120

baseplate protein

tail

YP_001595463.1

phrog_6

baseplate protein

tail

YP_001595464.1

phrog_587

structural protein

head and packaging

* Escherichia phage phiEcoM-GJ1 (Jamalludeen et al., 2008)

Biology

Viruses in the family Chaseviridae are obligately lytic and infect bacteria belonging to the phylum Proteobacteria, class Gammaproteobacteria and have a worldwide distribution.

Derivation of names

Cleopatravirinae: from Cleopatra VII Philopator (69 - 30 BCE) who was the last active ruler of the Ptolemaic Kingdom in Egypt.

Carltongylesvirus:  named in honour of Dr. Carlton Gyles University Professor Emeritus, University of Guelph, Ontario, Canada, in whose laboratory Escherichia phage phiEcoM-GJ1 was isolated and studied.

Chaseviridae – The family name honours Martha Cowles Chase (1927 – 2003), also known as Martha C. Epstein, an American geneticist known for experimentally confirming (with Alfred Hershey) that DNA rather than protein is the genetic material of life (https://en.wikipedia.org/wiki/Martha_Chase).

Faunusvirus: from the name of the exemplar isolate of the species Erwinia virus Faunus, Erwinia phage Faunus.

Loessnervirus: named in honour of  Prof. Dr. Martin J. Loessner, ETH Zurich, Switzerland, in whose laboratory Erwinia phage vB_EamM-Y2 was first isolated and studied.

Myducvirus: from the first virus of this genus, Proteus phage Myduc

Nefertitivirinae – from Neferneferuaten Nefertiti (c. 1370 – c. 1330 BCE) who was an Egyptian queen and the Great Royal Wife of Akhenaten, an Egyptian Pharaoh.

Pahsextavirus: from the first isolate of a virus from this genus, Aeromonas phage pAh6-C, with the number six replaced with the Latin prefix sexta.

Sabourvirus: named in honour of Dr. Parviz Sabour (Agriculture and AgriFood Canada emeritus scientist) who was the first AgroFood Canada scientist to carry out research on the agricultural application of bacteriophages.

Suwonvirus: This genus is named after Suwon, the capital of Gyeonggi Province, in north-western South Korea where Pectobacterium phage PM1 was first isolated.

Yushanvirus: from Yushan Road, the location of the Ocean University of China, College of Food Science & Engineering where Shewanella phage Spp001 was isolated.

Subfamily demarcation criteria

Subfamilies (Table 3.Chaseviridae) are identified as well-supported monophyletic groups based on phylogenetic analysis of the RNA polymerase and terminase large subunit proteins (Figure 3.Chaseviridae). Within each subfamily, members are 25–29% similar in their whole genome sequence as calculated with the VIRIDIC algorithm.

Table 3.Chaseviridae. The subfamilies of Chaseviridae

Subfamily

Genera

Hosts

Genome (kbp)*

Terminal repeats

Nefertitirinae

2

Aeromonas sp, Shewanella sp

52.48

 

ca. 3 kbp

Cleopatravirinae

6

Erwinia sp, Escherichia sp, Pantoea sp, Pectobacterium sp, Proteus sp

53.45

 

ND**

*Average; **ND Not determined for any member

 

Figure 3.Chaseviridae. Partitioned Maximum Likelihood phylogenetic tree of the RNA polymerase and terminase large subunit amino acid sequences of members of the family Chaseviridae. For each predicted protein, amino acid sequences were aligned with MAFFT (Katoh and Standley 2013), and trimmed with Trimal using the setting “gappyout” (Capella-Gutiérrez et al., 2009). The phylogenetic tree was constructed using the IQ-Tree suite, using the partitioned analysis with mixed data setting using as input the full multiple sequence alignment of each protein sequence with ultrafast bootstraps (UFBoot) calculated on 1000 repetitions (Nguyen et al., 2015, Chernomor et al., 2016, Hoang et al., 2018). For both genes, the best fitting substitution model was LG+G4 as determined using ModelFinder on each alignment separately, based on the Bayesian Information Criterion (Kalyaanamoorthy et al., 2017). The log-likelihood of the final tree was -18292. The consensus tree was drawn midpoint rooted with unclassified viruses indicated by open circles. UFBoot values above 95% are shown at nodes.  

Genus demarcation criteria

Genera in the family Chaseviridae are well-supported monophyletic clades by VIRIDIC clustering and in (concatenated) marker gene phylogenies. Members of a genus share at least 70% nucleotide identity across the genome. Members of the same genus generally infect members of the same bacterial genu

Species demarcation criteria

Members of the same species are more than 95% identical in genome nucleotide sequence, including the terminal repeat region. Viruses with genomes that differ by more than 5% are assigned to different species.  

Related unclassified viruses

Virus name

Accession No.

Reference

Erwinia phage pEa_SNUABM_27

MW349138

 

Escherichia phage vB_EcoP_Bp7

MN117721

 

Escherichia phage vB_EcoM_Bp10

MN122072

 

Aeromonas phage pAh6.2TG

MZ336020

 

Aeromonas phage PVN02

MT623578

 

Aeromonas phage PVN03

MW380983

 

Aeromonas phage PVN04

MW380984

 

Aeromonas phage PVN05

MW380985

 

Aeromonas phage PAS-1

JF342690, JF342689, JF342688, JF342687, JF342686, JF3426841, JF342683(*)

(Kim et al., 2012)

(*)  partial genome

Relationships within the family

A Maximum Likelihood tree for the RNA polymerase and terminase large subunit proteins (Figure 3.Chaseviridae) shows a clear separation between members of the two subfamilies Nefertitivirinae and Cleopatravirinae. Members of different genera are robustly separated into different clades. Within a genus, differences between members of different species are separated into reproducible clades as evidenced by short branch lengths and low bootstrap support. Nucleotide similarity over the entire genome length for species demarcation.

Relationships with other taxa

Viruses in the family Chaseviridae share morphological similarity with other myoviruses, i.e. dsDNA bacteriophages with contractile tails. A ViPTree which employs TBLASTx analyses shows deep branching of members of this family into two clades (Figure 4.Chaseviridae). 

Figure 4.Chaseviridae. ViPTree analysis (https://www.genome.jp/viptree/; (Nishimura et al., 2017)) is based upon the Phage Proteomic Tree (Rohwer and Edwards 2002). The tree was annotated in iTol (Letunic and Bork 2019) to display the virus families as a colour strip.  Members of the Chaseviridae are indicated in dark red. The tree scale as indicated with concentric circles represents the similarity between genomes at the predicted proteome level on a scale from 0 to 1 (branch length 0 = identical, 1 = no detectable similarity).

Member taxa