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Taxonomic
Note
Nomenclature and taxonomy of the genus
Salmonella
B. J. Tindall,
1
P. A. D. Grimont,
2
G. M. Garrity
3
and J. P. Euze
´
by
4
Correspondence
B. J. Tindall
bti@dsmz.de
1
DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder
Weg 1b, D-38124 Braunschweig, Germany
2
Unite
´
de Biodiversite
´
des Bacte
´
ries Pathoge
`
nes Emergentes, INSERM U389, Institut Pasteur,
F-75724 Paris Cedex 15, France
3
Bergey’s Manual Trust, Department of Microbiology and Molecular Genetics, 6162 Biomedical
Physical Sciences Bldg, Michigan State University, East Lansing, MI 48824-4320, USA
4
Socie
´
te
´
de Bacte
´
riologie Syste
´
matique et Ve
´
te
´
rinaire (SBSV) and Ecole Nationale Ve
´
te
´
rinaire
de Toulouse (ENVT), 23 Chemin des Capelles, BP 87614, F-31076 Toulouse Cedex 03,
France
The nomenclature of the genus Salmonella has reached an unsatisfactory state of affairs, with
two systems of nomenclature in circulation. One system, proposed in the 1980s by Le Minor
and Popoff, has received wide acceptance, although it does not conform to the rules of the
Bacteriological Code. The other system, which conforms to the rules of the Bacteriological Code,
is being used by an ever-decreasing minority. As a result of a number of recent Requests for an
Opinion, the Judicial Commission of the International Committee on the Systematics of Prokaryotes
has issued an Opinion (Opinion 80) with the intention that it should solve these discrepancies.
However, like all Opinions, it is limited to matters of nomenclature and does not help to interpret
the taxonomic consequences. The Judicial Commission has therefore asked experts in the field
of nomenclature and taxonomy to write a commentary on the nomenclatural and taxonomic
consequences of Opinion 80. The present article explains the nomenclatural consequences of
Opinion 80, together with a clear presentation of the taxonomy that results when applying the
currently widely accepted interpretation that the genus Salmonella currently includes only two
species.
The current taxonomy and nomenclature of the genus
Salmonella have been the subject of debate since Le Minor
& Popoff (1987) proposed changes in the 1980s. In their
Request for an Opinion, these authors not only proposed
changes in the nomenclature of the species of this genus,
but also requested that formal taxonomic interpretations
be taken into consideration. Their request to recognize a
single species could not be dealt with by the Judicial
Commission because the Commission may only act on
matters of nomenclature. Taxonomic opinion is not
governed by the Bacteriological Code (the Code).
The nomenclatural changes that were proposed dealt with
important human and animal pathogens. At the time, the
Judicial Commission could not predict whether these
changes would have severe consequences for the reporting
of disease caused by pathogens such as Salmonella typhi.
Following careful deliberations, the Judicial Commission
recommended that the authors reformulate their Request
for an Opinion to conform to the Code, but this did not
happen (Wayne, 1994). In the intervening years, the
nomenclature of Le Minor & Popoff (1987) has become
widely accepted in certain countries, despite the fact that
those names have not been validly published and have no
standing in nomenclature. In addition, their proposed
taxonomy is also now in common usage. Euze
´
by (1999),
Ezaki et al. (2000a, b) and Ezaki & Yabuuchi (2000) sub-
mitted proposals to deal with the problem of the serious
discrepancies between the nomenclature of Le Minor &
Popoff (1987) and that which is recognized under the
Code. The major problem at present is that two systems
of nomenclature are in use for members of the genus
Salmonella and that great care must be taken when attempts
are made to unify these systems. It was generally agreed
during the meeting of the Judicial Commission held in
2002 that a solution must be sought that provides a link
between the two nomenclatural systems while causing as
little confusion as possible. Recognizing that the average
microbiologist was not familiar with the Code, the com-
missioners believed that it would be necessary to deal
with the nomenclatural problem and to provide a guide as
to how the taxonomic consequences could be illustrated.
In publishing Opinion 80, the Judicial Commission (2005)
has sought to provide a solution to the problem of
63580
G
2005 IUMS Printed in Great Britain 521
International Journal of Systematic and Evolutionary Microbiology (2005), 55, 521–524 DOI 10.1099/ijs.0.63580-0
nomenclature in this genus. However, the Judicial Com-
mission does not have the power to rule on how these
nomenclatural changes will affect the taxonomy of this
group. In order to avoid confusion, it is the purpose of
the present article to provide a clear interpretation of the
nomenclature and taxonomy of members of the genus
Salmonella.
Prior to the publication of Opinion 80, the Code recognized
the following names as being validly published within the
genus Salmonella:
Salmonella choleraesuis (Smith 1894) Weldin 1927 (type
species of the genus), type strain ATCC 13312 =CIP 55.133
=NCTC 5735 =DSM 14846 =JCM 1651 (serovar
Choleraesuis),
Salmonella bongori (Le Minor et al. 1985) Reeves et al. 1989,
type strain ATCC 43975 =CCUG 30042 =CIP 82.33
=DSM 13772 =NCTC 12419,
Salmonella choleraesuis subsp. bongori Le Minor et al. 1985,
type strain ATCC 43975 =CCUG 30042 =CIP 82.33
=DSM 13772 =NCTC 12419,
Salmonella enteritidis (Gaertner 1888) Castellani and
Chalmers 1919, type strain ATCC 13076 =NCTC 12694,
Salmonella paratyphi (ex Kayser 1902) Ezaki et al. 2000, type
strain NCTC 5702 =KI 1015,
Salmonella typhi (Schroeter 1886) Warren and Scott 1930,
type strain ATCC 19430 =CUETM 79.394 =HAMBI 1306
=NCTC 8385,
Salmonella typhimurium (Loeffler 1892) Castellani and
Chalmers 1919, type strain ATCC 13311 =NCTC 74 =CIP
58.58 =JCM 1652 (serovar Typhimurium),
Salmonella choleraesuis subsp. choleraesuis (Smith 1894)
Weldin 1927, type strain ATCC 13312 =CIP 55.133 =NCTC
5735 =DSM 14846 =JCM 1651 (serovar Choleraesuis),
Salmonella arizonae (Borman 1957) Kauffmann 1964, type
strain ATCC 13314 =CCUG 6322 =CIP 82.30 =DSM
9386=NCTC 8297,
Salmonella choleraesuis subsp. arizonae (Borman 1957) Le
Minor et al. 1985, type strain ATCC 13314 =CCUG 6322
=CIP 82.30 =DSM 9386 =NCTC 8297,
Salmonella choleraesuis subsp. diarizonae Le Minor et al.
1985, type strain ATCC 43973 =CCUG 30040 =CIP 82.31
=NCTC 10060 =DSM 14847,
Salmonella choleraesuis subsp. houtenae Le Minor et al.
1985, type strain ATCC 43974 =CCUG 30041 =CIP 82.32
=DSM 9221 =NCTC 12418,
Salmonella choleraesuis subsp. indica Le Minor et al. 1987,
type strain K1240 =ATCC 43976 =CCUG 30038 = CIP
102501 =NCTC 12420 = DSM 14848, and
Salmonella choleraesuis subsp. salamae Le Minor et al.
1985, type strain ATCC 43972 =CCUG 30039 =CIP 8229
=DSM 9220 =NCTC 5773.
Le Minor & Popoff (1987) proposed that the type species
of the genus Salmonella should be changed to Salmonella
enterica, with the type strain of that species being strain LT2.
The authors did not exclude the fact that other authors
may wish to retain other names that were validly published:
‘Since we recognize the right of other bacteriologists to
believe that the genus Salmonella should be composed of
several species, including S. choleraesuis, we shall refrain
from requesting the rejection of that name.’
In reacting to the Requests for an Opinion by Ezaki et al.
(2000a, b) and Euze
´
by (1999), the Judicial Commission
has also taken the request of Le Minor & Popoff (1987)
into consideration and decided that Salmonella enterica
becomes the type species of the genus, replacing Salmonella
choleraesuis (Judicial Commission, 2005). The type strain
of Salmonella enterica is CIP 60.62 =NCIMB 11450 =
LT2 =ATCC 43971 =NCTC 12416. Furthermore, to avoid
any ambiguities in interpreting the Code, the epithet enterica
in Salmonella enterica is conserved over all earlier epithets
that may be applied to this species. The Judicial Commission
has also ruled that the subspecies combinations proposed
by these authors should also be considered to be validly
published, with the dates and authorship being assigned to
these authors. In proposing these subspecies, Salmonella
enterica subsp. enterica is automatically created (Rule 40d/
46). The circumscription of Salmonella enterica is given by
Le Minor & Popoff (1987) and also applies to Salmonella
enterica subsp. enterica. However, this also means that the
following names are validly published:
Salmonella enterica Le Minor and Popoff 1987 (type species
of the genus), type strain CIP 60.62 =NCIMB 11450 =LT2
=ATCC 43971 =NCTC 12416 (serovar Typhimurium),
Salmonella bongori (Le Minor et al. 1985) Reeves et al.
1989, type strain ATCC 43975 =CCUG 30042 =CIP 82.33
=DSM 13772 =NCTC 12419,
Salmonella enterica subsp. bongori (Le Minor et al. 1985) Le
Minor and Popoff 1987, type strain ATCC 43975 =CCUG
30042 =CIP 82.33 =DSM 13772 =NCTC 12419,
Salmonella choleraesuis subsp. bongori Le Minor et al. 1985,
type strain ATCC 43975 =CCUG 30042 =CIP 82.33
=DSM 13772 =NCTC 12419,
Salmonella enterica subsp. enterica Le Minor and Popoff
1987, type strain CIP 60.62 =NCIMB 11450 =LT2
=ATCC 43971 =NCTC 12416 (serovar Typhimurium),
Salmonella enteritidis (Gaertner 1888) Castellani and
Chalmers 1919, type strain ATCC 13076 =NCTC 12694,
Salmonella paratyphi (ex Kayser 1902) Ezaki et al. 2000,
type strain NCTC 5702 =KI 1015,
522 International Journal of Systematic and Evolutionary Microbiology 55
B. J. Tindall and others
Salmonella typhi (Schroeter 1886) Warren and Scott 1930,
type strain ATCC 19430 =CUETM 79.394 =HAMBI 1306
=NCTC 8385,
Salmonella typhimurium (Loeffler 1892) Castellani and
Chalmers 1919 (type strain ATCC 13311 =NCTC 74 =CIP
58.58 =JCM 1652 (serovar Typhimurium),
Salmonella choleraesuis (Smith 1894) Weldin 1927, type
strain ATCC 13312 =CIP 55.133 =NCTC 5735 =DSM
14846 =JCM 1651 (serovar Choleraesuis),
Salmonella choleraesuis subsp. choleraesuis (Smith 1894)
Weldin 1927, type strain ATCC 13312 =CIP 55.133 =NCTC
5735 =DSM 14846 =JCM 1651 (serovar Choleraesuis),
Salmonella enterica subsp. arizonae (Borman 1957) Le
Minor and Popoff 1987, type strain ATCC 13314 =CCUG
6322 =CIP 82.30 =DSM 9386 =NCTC 8297,
Salmonella arizonae (Borman 1957) Kauffmann 1964, type
strain ATCC 13314 =CCUG 6322 =CIP 82.30 =DSM
9386 =NCTC 8297,
Salmonella choleraesuis subsp. arizonae (Borman 1957) Le
Minor et al. 1985, type strain ATCC 13314 =CCUG 6322
=CIP 82.30 =DSM 9386 =NCTC 8297,
Salmonella enterica subsp. diarizonae (Le Minor et al. 1985)
Le Minor and Popoff 1987 1985, type strain ATCC 43973
=CCUG 30040 =CIP 82.31 =NCTC 10060 =DSM
14847,
Salmonella choleraesuis subsp. diarizonae Le Minor et al.
1985, type strain ATCC 43973 =CCUG 30040 =CIP 82.31
=NCTC 10060 =DSM 14847,
Salmonella enterica subsp. houtenae (Le Minor et al. 1985)
Le Minor and Popoff 1987, type strain ATCC 43974
=CCUG 30041 =CIP 82.32 = DSM 9221 =NCTC 12418,
Salmonella choleraesuis subsp. houtenae Le Minor et al.
1985, type strain ATCC 43974 =CCUG 30041 =CIP 82.32
=DSM 9221 =NCTC 12418,
Salmonella enterica subsp. indica (Le Minor et al . 1987)
Le Minor and Popoff 1987, type strain K1240 =ATCC
43976 =CCUG 30038 =CIP 102501 =NCTC 12420 =DSM
14848,
Salmonella choleraesuis subsp. indica Le Minor et al. 1987,
type strain K1240 =ATCC 43976 =CCUG 30038 = CIP
102501 =NCTC 12420 = DSM 14848,
Salmonella enterica subsp. salamae (Le Minor et al. 1985)
Le Minor and Popoff 1987 1985, type strain ATCC 43972
=CCUG 30039 =CIP 8229 =DSM 9220 =NCTC 5773,
and
Salmonella choleraesuis subsp. salamae Le Minor et al. 1985,
type strain ATCC 43972=CCUG 30039=CIP 8229=DSM
9220=NCTC 5773.
However, this does not appear to solve the current problems
of nomenclature, nor the different taxonomic interpreta-
tions. This is primarily due to the fact that the Judicial
Commission is not empowered by the Code as a taxonomic
arbiter [see Principle 1 (4)]. However, it is evident that, if
the taxonomic proposals of Le Minor & Popoff (1987) and
Reeves et al. (1989) are followed, only two species are to be
recognized. The Judicial Commission (2005) has ruled that
the type species of the genus Salmonella Lignieres 1900 is
Salmonella enterica Le Minor and Popoff 1987 and that the
epithet enterica be conserved over all earlier epithets that
may be applied to this species. At the same time, Le Minor &
Popoff (1987) also recognized that the species Salmonella
enterica be divided into several subspecies. Thus, by applying
the recent ruling of the Judicial Commission (2005) together
with the taxonomic interpretation of Le Minor & Popoff
(1987) and Reeves et al. (1989), the taxonomy and resulting
nomenclature that should be followed are listed below.
Those names that are to be used within the resulting
taxonomy are underlined.
Salmonella enterica (ex Kauffmann and Edwards 1952)
Le Minor and Popoff 1987 (type species of the genus),
type strain CIP 60.62 =NCIMB 11450 =LT2 =ATCC
43971 =NCTC 12416 (serovar Typhimurium),
=Salmonella choleraesuis (Smith 1894) Weldin 1927
(heterotypic synonym), type strain ATCC 13312 =CIP
55.133 =NCTC 5735 =DSM 14846 =JCM 1651 (serovar
Choleraesuis),
Salmonella bongori (Le Minor et al. 1985) Reeves et al. 1989,
=Salmonella enterica subsp. bongori (Le Minor et al. 1985)
Le Minor and Popoff 1987 (homotypic synonym)
=Salmonella choleraesuis subsp. bongori Le Minor et al.
1985 (homotypic synonym), type strain ATCC 43975 =
CCUG 30042 =CIP 82.33 =DSM 13772 =NCTC 12419,
Salmonella enterica subsp. enteri ca (ex Kauffmann and
Edwards 1952) Le Minor and Popoff 1987, type strain CIP
60.62 =NCIMB 11450 =LT2 =ATCC 43971 =NCTC
12416 (serovar Typhimurium),
=Salmonella enteritidis (Gaertner 1888) Castellani and
Chalmers 1919 (heterotypic synonym), type strain ATCC
13076 =NCTC 12694,
=Salmonella paratyphi (ex Kayser 1902) Ezaki et al. 2000
(heterotypic synonym), type strain NCTC 5702=KI 1015,
=Salmonella typhi (Schroeter 1886) Warren and Scott 1930
(heterotypic synonym), type strain ATCC 19430 =CUETM
79.394=HAMBI 1306 =NCTC 8385,
=Salmonella typhimurium (Loeffler 1892) Castellani and
Chalmers 1919 (heterotypic synonym), type strain ATCC
13311 =NCTC 74 =CIP 58.58 =JCM 1652 (serovar
Typhimurium),
http://ijs.sgmjournals.org 523
Taxonomy and nomenclature of the genus Salmonella
=Salmonella choleraesuis subsp. choleraesuis (Smith 1894)
Weldin 1927 (heterotypic synonym), type strain ATCC
13312 =CIP 55.133 =NCTC 5735 =DSM 14846 =JCM
1651 (serovar Choleraesuis),
Salmonella enterica subsp. arizonae (Borman 1957) Le
Minor and Popoff 1987,
=Salmonella arizonae (Borman 1957) Kauffmann 1964
(homotypic synonym) =Salmonella choleraesuis subsp.
arizonae (Borman 1957) Le Minor et al. 1985 (homotypic
synonym), type strain ATCC 13314 =CCUG 6322 =CIP
82.30 =DSM 9386 =NCTC 8297,
Salmonella enterica subsp. diarizonae (Le Minor et al. 1985)
Le Minor and Popoff 1987,
=Salmonella choleraesuis subsp. diarizonae Le Minor et al.
1985 (homotypic synonym), type strain ATCC 43973
=CCUG 30040 =CIP 82.31 =NCTC 10060 =DSM 14847,
Salmonella enterica subsp. houtenae (Le Minor et al. 1985) Le
Minor and Popoff 1987,
=Salmonella choleraesuis subsp. houtenae Le Minor et al.
1985 (homotypic synonym), type strain ATCC 43974
=CCUG 30041 =CIP 82.32 = DSM 9221 =NCTC 12418,
Salmonella enterica subsp. indica (Le Minor et al. 1987) Le
Minor and Popoff 1987,
=Salmonella choleraesuis subsp. indica Le Minor et al.
1987 (homotypic synonym), type strain K1240 =ATCC
43976 =CCUG 30038 =CIP 102501 =NCTC 12420
=DSM 14848, and
Salmonella enterica subsp. salamae (Le Minor et al. 1985) Le
Minor and Popoff 1987,
=Salmonella choleraesuis subsp. salamae Le Minor et al.
1985 (homotypic synonym), type strain ATCC 43972
=CCUG 30039 = CIP 8229 =DSM 9220 =NCTC 5773.
It is hoped that the recent actions of the Judicial Com-
mission (2005) have allowed the nomenclatural changes
envisaged by Le Minor & Popoff (1987) to take effect. In
addition, the taxonomic opinion of Le Minor et al. (1982),
Le Minor & Popoff (1987) and Reeves et al. (1989), that the
genus Salmonella should currently comprise two species
and that the type species Salmonella enterica should be
divided into six subspecies, results in the taxonomy and
nomenclature currently in use by the WHO and other
organizations. It is now hoped that the resulting taxonomy
and nomenclature will find widespread usage.
References
Euze
´
by, J. P. (1999). Revised Salmonella nomenclature: designation
of Salmonella enterica (ex Kauffmann and Edwards 1952) Le Minor
and Popoff 1987 sp. nov., nom. rev. as the neotype species of the
genus Salmonella Lignieres 1900 (Approved Lists 1980), rejection
of the name Salmonella choleraesuis (Smith 1894) Weldin 1927
(Approved Lists 1980), and conservation of the name Salmonella
typhi (Schroeter 1886) Warren and Scott 1930 (Approved Lists
1980). Request for an Opinion. Int J Syst Bacteriol 49, 927–930.
Ezaki, T., Amano, M., Kawamura, Y. & Yabuuchi, E. (2000a).
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an Opinion to conserve the specific epithet paratyphi in the binary
combination Salmonella paratyphi as nomen epitheton conservandum.
Int J Syst Evol Microbiol 50, 941–944.
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Salmonella Lignieres 1900 is Salmonella enterica (ex Kauffmann
and Edwards 1952) Le Minor and Popoff 1987, with the type strain
LT2
T
, and conservation of the epithet enterica in Salmonella enterica
over all earlier epithets that may be applied to this species. Opinion
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ron, M. & Popoff, M. Y. (1982). Proposition pour
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ron, M. & Popoff, M. Y. (1985). Salmonella cholerae-
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