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VIROLOGY DIVISION NEWS
Taxonomy of prokaryotic viruses: update from the ICTV
bacterial and archaeal viruses subcommittee
Mart Krupovic
1
•Bas E. Dutilh
2,3,4
•Evelien M. Adriaenssens
5
•
Johannes Wittmann
6
•Finn K. Vogensen
7
•Mathew B. Sullivan
8,9
•
Janis Rumnieks
10
•David Prangishvili
1
•Rob Lavigne
11
•Andrew M. Kropinski
22
•
Jochen Klumpp
12
•Annika Gillis
13
•Francois Enault
14,15
•Rob A. Edwards
16
•
Siobain Duffy
17
•Martha R. C. Clokie
18
•Jakub Barylski
19
•Hans-Wolfgang Ackermann
20
•
Jens H. Kuhn
21
Received: 10 December 2015 / Accepted: 12 December 2015
ÓSpringer-Verlag Wien (Outside the USA) 2016
The prokaryotic virus community is represented on the
International Committee on Taxonomy of Viruses (ICTV)
by the Bacterial and Archaeal Viruses Subcommittee. In
2008, the three caudoviral families Myoviridae, Podoviri-
dae, and Siphoviridae included only 18 genera and 36
species. Under the able chairmanship of Rob Lavigne (KU
Leuven, Belgium), major advances were made in the
classification of prokaryotic viruses and the order Cau-
dovirales was expanded dramatically, to reflect the
genome-based relationships between phages. Today, the
order includes six subfamilies, 80 genera, and 441 species.
This year, additional changes in prokaryotic virus taxon-
omy have been brought forward under the new subcom-
mittee chair, Andrew M. Kropinski (University of Guelph,
Canada). These changes are:
1. replacement of ‘‘phage’’ with ‘‘virus’’ in prokaryotic
virus taxon names. In recognition of the fact that
phages are first and foremost genuine viruses, and to
adhere to ICTV’s International Code of Virus Classi-
fication and Nomenclature (ICVCN), the word
‘‘phage’’ will disappear from taxon names, but not
from phage names. For instance, the current taxon
Escherichia phage T4 will be renamed Escherichia
virus T4, while the name of this taxon’s member will
remain unchanged (Escherichia phage T4). It is
The content of this publication does not necessarily reflect the views
or policies of the US Department of Health and Human Services, or
the institutions and companies affiliated with the authors. The
taxonomic changes summarized here have been submitted as official
taxonomic proposals to the International Committee on Taxonomy of
Viruses (ICTV) (www.ictvonline.org) and are by now accepted, but
not yet ratified. These changes therefore may differ from any new
taxonomy that is ultimately approved by the ICTV.
&Andrew M. Kropinski
Phage.Canada@gmail.com
Jens H. Kuhn
kuhnjens@mail.nih.gov
1
Unit of Molecular Biology of the Gene in Extremophiles,
Department of Microbiology, Institut Pasteur, 25 rue du Dr
Roux, 75015 Paris, France
2
Theoretical Biology and Bioinformatics, Utrecht University,
Utrecht, The Netherlands
3
Centre for Molecular and Biomolecular Informatics,
Radboud University, Medical Centre, Nijmegen,
The Netherlands
4
Instituto de Biologia, Universidade Federal do Rio de Janeiro,
Rio de Janeiro, Brazil
5
Department of Genetics, Centre for Microbial Ecology and
Genomics, University of Pretoria, Private Bag X20, Hatfield,
Pretoria 0028, South Africa
6
Leibniz-Institut DSMZ-Deutsche Sammlung von
Mikroorganismen und Zellkulturen GmbH, Inhoffenstraße
7B, 38124 Braunschweig, Germany
7
Department of Food Science, University of Copenhagen,
Rolighedsvej 26, 1958 Frederiksberg C, Denmark
8
Department of Microbiology, Ohio State University,
496 W 12th Ave, Columbus, OH 43210, USA
9
Department of Civil, Environmental, and Geodetic
Engineering, Ohio State University, 470 Hitchcock Hall,
2070 Neil Avenue, Columbus, OH 43210, USA
10
Latvian Biomedical Research and Study Center, Ra¯tsupı¯tes 1,
Riga, LV 1067, Latvia
11
Laboratory of Gene Technology, KU Leuven, Kasteelpark
Arenberg 21-box 2462, 3001 Leuven, Belgium
12
Institute of Food, Nutrition and Health, ETH Zurich,
Schmelzbergstrasse 7, 8092 Zurich, Switzerland
123
Arch Virol
DOI 10.1007/s00705-015-2728-0
important that the community remembers the ICVCN
distinction between viral taxa (such as species, genera,
families, or orders) and their members, the actual
viruses/phages: ‘‘viruses are real physical entities
produced by biological evolution and genetics,
whereas virus species and higher taxa are abstract
concepts produced by rational thought and logic’’;
2. elimination of the infix ‘‘like’’ from prokaryotic
virus genus names. The naming of phage taxa has
been an evolving process with genus names in the
form ‘‘P22-like virus’’, which was always considered
to be a stop-gap measure, being replaced by P22like-
virus. However, the latter convention is also prob-
lematic since it was only applied to genera included
in the order Caudovirales, and the infix ‘‘like’’ was
unnecessary since the grouping of viruses in genera
implies per se that their constituent members are
alike. Consequently, the infix ‘‘like’’ will be removed
from the names of phage genera and genus names
such as Lambdalikevirus and T4likevirus will become
Lambdavirus and T4virus, respectively. It will of
course remain correct to refer to ‘‘lambda-like
viruses’’ and ‘‘T4-like phages’’ during discussions
regarding specific groups of phages classified in these
taxa. There have also been discussions in the
Subcommittee whether all prokaryotic virus genera
should adopt the system used for some archaeal and
eukaryotic viruses, in which names of genera are
created from the root of the corresponding family
name with sequentially appended transliterated Greek
letters (e.g., Alphabaculovirus,Betabaculovirus, etc.).
However, it was decided that recognition of new
genus names is of paramount importance and that
further drastic changes in one setting might overly
confuse the community. Thus, in most cases, the infix
‘‘like’’ was merely removed and the name of the
founding member of the genus was retained as a root
of the taxon name;
3. discontinuation of the use of ‘‘Phi’’ and other
transliterated Greek letters in the naming of new
prokaryotic virus genera. Since some scientists are
under the impression that ‘‘Phi’’ in its various forms
(phi, u,U) indicates a phage, over the years, many
phages were given names containing the prefix ‘‘Phi’’ .
However, the prefix ‘‘Phi’’ adds no informational value
when naming phage genera. Consequently, the Sub-
committee decided that, unless there was sufficient
historical precedent (e.g., U29 or UX174), Phi would
no longer be added to genus names. In addition, Greek
letters can create problems in electronic databases, as
exemplified by a PubMed search for references on
Bacillus phage U29 [1], which retrieved articles on phi
29, phi29, Phi 29, Phi29, 29 phi, {phi}29, u29, and
u29 phages. Therefore, the Subcommittee strongly
discourages phage scientists from using Phi or any
other Greek letter in virus and virus taxon names in the
future;
4. elimination of hyphens from taxon names. The
ICVCN discourages hyphens in virus taxon names.
Accordingly, taxon names such as Yersinia phage
L-413C have been renamed (in this instance to Yersinia
virus L413C). However, hyphens are retained when
appearing in a number string: Thermus phage P2345
becomes Thermus virus P23-45 (its correct name) [2].
5. inclusion of the isolation host name in the taxon
name. On several occasions, terms such as ‘‘Enter-
obacteria’’ o r ‘‘ Pseudomonad’’ have been used in
phage taxon names. However, such terms do not refer
to a specific bacterial host; nor do they indicate
whether the phage in question was tested upon a
variety of members of the particular host group. To
improve the situation, terms such as ‘‘Enterobacteria’’
13
Laboratory of Food and Environmental Microbiology,
Universite
´catholique de Louvain, Croix du Sud 2, L7.05.12,
1348 Louvain-la-Neuve, Belgium
14
Clermont Universite
´, Universite
´Blaise Pascal,
Laboratoire ‘‘Microorganismes: Ge
´nome et Environnement’’,
Clermont-Ferrand, France
15
CNRS UMR 6023, LMGE, Aubie
`re, France
16
Bioinformatics Lab, Department of Computer Science, San
Diego State University, 5500 Campanile Drive, San Diego,
CA 92182-7720, USA
17
Department of Ecology, Evolution and Natural Resources,
Rutgers University, 14 College Farm Rd, New Brunswick,
NJ 08901, USA
18
Department of Infection, Immunity and Inflammation,
University of Leicester, University Road,
Leicester LE1 9HN, UK
19
Department of Molecular Virology, Institute of Experimental
Biology, Adam Mickiewicz University, Umultowska 89,
61-614 Poznan, Poland
20
L’Institut de biologie inte
´grative et des systems, Universite
´
Laval, Pavillon Charles-Euge
`ne-Marchand, 1030, avenue de
la Me
´decine, Quebec, QC G1V 0A6, Canada
21
Integrated Research Facility at Fort Detrick, National
Institute of Allergy and Infectious Diseases, National
Institutes of Health, Fort Detrick, Frederick, MD 21702, USA
22
Departments of Food Science, Molecular and Cellular
Biology, and Pathobiology, University of Guelph, 50 Stone
Rd E, Guelph, ON N1G 2W1, Canada
M. Krupovic et al.
123
Table 1 Taxonomy proposals describing new taxa (genera, subfamilies, families) submitted to the ICTV in 2015
New genus Family Subfamily Type species Number of
genus-included
species
Ap22virus Myoviridae Acinetobacter virus AP22 4
Secunda5virus Myoviridae Aeromonas virus 25 5
Biquartavirus Myoviridae Aeromonas virus 44RR2 1
Agatevirus Myoviridae Bacillus virus Agate 3
B4virus Myoviridae Bacillus virus B4 5
Bastillevirus Myoviridae Bacillus virus Bastille 2
Bv431virus Myoviridae Bacillus virus Bc431 4
Cp51virus Myoviridae Bacillus virus CP51 3
Nit1virus Myoviridae Bacillus virus NIT1 3
Wphvirus Myoviridae Bacillus virus WPh 1
Cvm10virus Myoviridae Escherichia virus CVM10 2
Kpp10virus Myoviridae Pseudomonas virus KPP10 3
Pakpunavirus Myoviridae Pseudomonas virus PAKP1 6
Rheph4virus Myoviridae Rhizobium virus RHEph4 1
Vhmlvirus Myoviridae Vibrio virus VHML 3
Tg1virus Myoviridae Yersinia virus TG1 2
P100virus Myoviridae Spounavirinae Listeria virus P100 1
Kayvirus Myoviridae Spounavirinae Staphylococcus virus K 7
Silviavirus Myoviridae Spounavirinae Staphylococcus virus Remus 2
Rb49virus Myoviridae Tevenvirinae Escherichia virus RB49 3
Rb69virus Myoviridae Tevenvirinae Escherichia virus RB69 4
Js98virus Myoviridae Tevenvirinae Escherichia virus JS98 5
Sp18virus Myoviridae Tevenvirinae Shigella virus SP18 5
S16virus Myoviridae Tevenvirinae Salmonella virus S16 2
Cc31virus Myoviridae Tevenvirinae Enterobacter virus CC31 2
Cr3virus Myoviridae Vequintavirinae (new) Cronobacter virus CR3 3
V5virus Myoviridae Vequintavirinae (new) Escherichia virus V5 4
Se1virus Myoviridae Vequintavirinae (new) Salmonella virus SE1 4
Pagevirus Podoviridae Bacillus virus Page 5
Cba41virus Podoviridae Cellulophaga virus Cba41 2
G7cvirus Podoviridae Escherichia virus G7C 8
Lit1virus Podoviridae Pseudomonas virus LIT1 3
Vp5virus Podoviridae Vibrio virus VP5 3
Kp34virus Podoviridae Autographivirinae Klebsiella virus KP34 5
Slashvirus Siphoviridae Bacillus virus Slash 4
Cba181virus Siphoviridae Cellulophaga virus Cba181 3
Cbastvirus Siphoviridae Cellulophaga virus ST 1
Nonagvirus Siphoviridae Escherichia virus 9g 4
Seuratvirus Siphoviridae Escherichia virus Seurat 2
P70virus Siphoviridae Listeria virus P70 5
Psavirus Siphoviridae Listeria virus PSA 2
Ff47virus Siphoviridae Mycobacterium virus Ff47 2
Sitaravirus Siphoviridae Paenibacillus virus Diva 5
Septima3virus Siphoviridae Pseudomonas virus 73 5
Nonanavirus Siphoviridae Salmonella virus 9NA 2
Sextaecvirus Siphoviridae Staphylococcus virus 6ec 2
Ssp2virus Siphoviridae Vibrio virus SSP002 2
Prokaryotic virus taxonomy
123
or ‘‘Pseudomonad’’ in taxon names will be replaced
with the isolation host genus name: for instance,
Enterobacteria phage T7 will become Escherichia
virus T7. In addition, host species names will be
eliminated from taxon names. For example, Thermus
thermophilus phage IN93 will become Thermus virus
IN93.
Further considerations
DNA-DNA relatedness is the gold standard in the classi-
fication of all prokaryotes [3–7], and efforts are underway
to move towards a completely genomic taxonomy in that
field [8]. The Bacterial and Archaeal Viruses Subcommit-
tee has previously used overall proteome similarity to
define genera and subfamilies, with 40 % homologous
proteins indicating membership in the same genus [9–11].
This has resulted in spurious taxonomic lumping [12–14].
Furthermore, EMBOSS Stretcher [15,16], which has been
used for calculating nucleotide similarities between related
phages (e.g., [17]), suffers from certain limitations (in
particular the requirement for the genomes to be collinear).
Problems with EMBOSS Stretcher are highlighted when an
alignment of the phage T7 genome with a randomly
shuffled T7 DNA sequence (http://www.bioinformatics.
org/sms2/shuffle_dna.html) is attempted. The resulting
value, 47.6 % identity, demonstrates that EMBOSS
Stretcher values below a certain threshold are meaningless.
Accordingly, more recent phage classification efforts have
explored alternative approaches. Specifically, BLASTN
[19] was found to be superior to EMBOSS Stretcher for
identification and quantitative comparison of closely rela-
ted phages [16]. Indeed, a BLASTN search seeded with the
shuffled sequence of phage T7 specifically against ‘‘En-
terobacteria phage T7’’ results in no detectable similarity,
as expected from a randomized sequence with 48.4 % GC
content. Moreover, BLASTN has also been used to deter-
mine relationships between phages at larger phylogenetic
distances [17,18], although the meaning of a similarity
search hit in the absence of a true-shared ancestry remains
unclear. Most of the newer programs that calculate phy-
logenetic relationships between genome sequences,
including CLANS [20], GEGENEES [21], and mVISTA
[22], are based upon sequence similarity analyses such as
provided by BLASTN [19]. Complete and near-complete
viral genome and protein homologies will be the focus of
the Bacterial and Archaeal Viruses Subcommittee’s atten-
tion in 2016 to develop clearer parameters for the molec-
ular definition of genera, subfamilies, and families.
The changes described here were formalized and sub-
mitted in more than 40 ICTV taxonomic proposals (Tax-
oProps) for consideration by the ICTV Executive
Committee (http://www.ictvonline.org/). One new archaeal
virus family (Pleolipoviridae), four new bacterial sub-
families (Guernseyvirinae [Salmonella phage Jersey], Ve-
quintavirinae [Escherichia phage rV5], Tunavirinae
[Escherichia phage T1], and Bullavirinae [Escherichia
phage UX174]), and 59 new genera including 232 species
are covered in these proposals (summarized in Table 1).
While the Bacterial and Archaeal Viruses Subcommittee
is delighted with the progress described here, some
400–600 new genomes of novel phages are deposited to
Table 1 continued
New genus Family Subfamily Type species Number of
genus-included
species
K1gvirus Siphoviridae Guernseyvirinae (new) Escherichia virus K1G 4
Jerseyvirus (existing) Siphoviridae Guernseyvirinae (new) Salmonella virus Jersey 6
Sp31virus Siphoviridae Guernseyvirinae (new) Salmonella virus SP31 1
T1virus (existing) Siphoviridae Tunavirinae (new) Escherichia virus T1 4
Tlsvirus Siphoviridae Tunavirinae (new) Escherichia virus TLS 3
Rtpvirus Siphoviridae Tunavirinae (new) Escherichia virus Rtp 2
Kp36virus Siphoviridae Tunavirinae (new) Klebsiella virus KP36 3
Rogue1virus Siphoviridae Tunavirinae (new) Escherichia virus Rogue1 8
Alpha3microvirus Microviridae Bullavirinae (new) Escherichia virus alpha3 8
G4microvirus Microviridae Bullavirinae (new) Escherichia virus G4 3
Phix174microvirus Microviridae Bullavirinae (new) Escherichia virus phiX174 1
Alphapleolipovirus Pleolipoviridae (new) Halorubrum virus HRPV-1 5
Betapleolipovirus Pleolipoviridae (new) Halorubrum virus HRPV-3 2
Gammapleolipovirus Pleolipoviridae (new) Haloarcula virus His2 1
M. Krupovic et al.
123
GenBank annually. Many of these may have to be assigned
to novel species or higher taxa via the ICTV TaxoProp
process. Phage classification will therefore remain a highly
demanding and daunting process, unless a genomic tax-
onomy for viruses is embraced (see [8]). Although a tax-
onomy that is based on the genome sequence alone might
be incorrect due to rampant genomic rearrangements in
viruses [23], such an approach may turn out to be the only
scalable solution.
Compliance with ethical standards
Funding This work was funded in part through Battelle Memorial
Institute’s prime contract with the US National Institute of Allergy
and Infectious Diseases (NIAID) under Contract No.
HHSN272200700016I. A subcontractor to Battelle Memorial Institute
who performed this work is: J.H.K., an employee of Tunnell
Government Services, Inc. B.E.D. was supported by the Netherlands
Organization for Scientific Research (NWO) Vidi Grant 864.14.004
and CAPES/BRASIL.
Conflict of interest The authors declare that they have no conflict
of interest.
Ethical approval This article does not contain any studies with
human participants or animals performed by any of the authors.
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