INTERNATIONAL
JOURNALOF SYSTEMATIC
BACTERIOLOGY,
Oct. 1987, p. 465-468
0020-7713/87/040465-04$02.00/0
Copyright 0 1987, International Union of Microbiological Societies
Vol. 37, No. 4
Request for an Opinion
Designation of Salmonella enterica sp. nov., norn. rev., as the Type
and Only Species of the Genus Salmonella
LEON LE MINOR* A N D MICHEL Y. POPOFF
WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur,
F-75724 Paris Cedex 15, France
Since the publication of the Approved Lists of Bacterial Names, the type species of the genus Salmonella has
been S . choleraesuis. At the time of publication of the Approved Lists, five Salmonella species had standing in
the nomenclature, and the description of S. choleraesuis was the same as that of the serotype of that name.
Several studies have shown that the genus Salmonella consists of only one species, and the strict application of
the Bacteriological Code would recognize S. choleraesuis (the type species) as the single Salmonella species. This
can lead to confusion and hazards since the specific epithet is also the name of a serovar (serovar Choleraesuis).
This confusion is increased by the common practice of using serovar names as if they represented species names
(e.g., S. typhi, S. choleraesuis, and S . typhimurium). Some serovars (e.g., Salmonella choleraesuis subsp.
choleraesuis serovar Typhi) are highly pathogenic and cause a disease different from that caused by other
serovars (e.g. S. choleraesuis subsp. choleraesuis serovar Choleraesuis). To avoid further confusion, it is
proposed to use for the single Salmonella species a name which has not been used earlier for a serotype. It is
thus requested that the type species of the genus Salmonella be Salmonella enterica sp. nov., nom. rev. with
strain CIP 60.62 (a H2S-producing clone of strain LT2) as the type strain. Since the name S. choleraesuis is not
proposed for rejection, bacteriologists who do not accept the single species concept of the genus Salmonella will
be free to use the name S. choleraesuis as a synonym of Salmonella enterica subsp. enterica serotype
Choleraesuis.
The species concept in the genus Salmonella has evolved
in four overlapping phases. Each of these phases relied on
available methodology and knowledge stressing (i) clinical
evidence, (ii) antigenic specificities, (iii) biochemical properties and (iv) deoxyribonucleic acid (DNA) relatedness.
species be recognized: S . choleraesuis, “ S . typhosa,” and
“ S . kaufimannii.” This last species included all serovars
other than the first two. A similar proposal was made in 1952
by Kauffmann and Edwards (14), who then recognized three
species: S . choleraesuis, “ S . typhosa,” and “ S . enterica.”
Ewing in 1963 (5) recognized S . choleraesuis, S . typhi, and
S . enteritidis. Consequently, all serovars except S . choleraesuis and S . typhi belonged to S . enteritidis.
Later, Kauffmann (15, 17, 18) divided the genus Salmonella on the basis of biochemical characteristics into four
subgenera (I to IV) without making a formal nomenclature
proposal, and continued to apply his concept of “one
serovar-one species. Nevertheless, phenotypic studies and
numerical taxonomy (12, 34, 35) showed that, apart from
host-adapted serovars (e.g., S . typhi and “ S . paratyphi A”),
Salmonella serovars within each subgenus were biochemically indistinguishable. For this reason, Kauffmann’s
subgenera were considered to be species (22): “ S . kauflmannii” (subgenus I), “ S . salamae” (subgenus 11), S .
arizonae (subgenus 111), and “ S . houtenae” (subgenus IV).
The Approved Lists (30) included five Salmonella species:
S . arizonae, S . choleraesuis, S . enteritidis, S . typhi, and S.
typhimurium.
Taxonomy based on DNA relatedness. DNA relatedness
studies demonstrated that all Salmonella serovars formed a
single DNA hybridization group with seven subgroups delineated by studies of the thermal stability of hybrids (4, 21,
23, 33). The level of DNA relatedness among DNA subgroups generally was consistent with that of subspecies
within one single Salmonella species, although subgroup V
(Bongor) was somewhat less related and could possibly
represent a second species (23). Therefore, all five species
listed in the Approved Lists (30) are members of a single
Taxonomy based on the clinical role of Salmonella strains.
Strains were considered different species when isolated from
different clinical conditions (e.g., “Eberthella typhosa” or
S . typhi and S . enteritidis) or different hosts ( “ S .
abortusovis,” “ S . gallinarum-pullorum,” and S . choleraesuis). It was soon realized that a number of these so-called
species were ubiquitous, and emphasis shifted to antigenic
properties.
Taxonomy based on antigenic specificities. Serological analysis of 0 and H antigens initiated by White (36) and
continued and extended by Kauffmann (17) resulted in the
description of a great number of serovars. In 1961, Kauffmann (16) defined the species as “a group of related serofermentative phage types,” with the result that each Salmonella serovar was considered as a species. This “one
serovar-one species” concept is untenable. It should be
noted that more than 2,100 serovars have been described.
Since some names inferring a host specificity happened to be
bad choices, epithets of the new serovars were later derived
from the geographic location where the first strain was
isolated (e.g., “ S . panama” and “S. montevideo”).
Taxonomy based on biochemical properties. Most serovars
cannot be separated by biochemical tests, and several authors have made proposals aimed at reducing the number of
species. In 1944, Borman et al. (2) proposed that only three
”
* Corresponding author
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INT. J . SYST.BACTERIOL.
LE MINOR AND POPOFF
genospecies. The correlation between DNA subgroups and
Kauffmann’s subgenera was close except that subgenus I11
was split in two DNA subgroups containing monophasic
serovars (IIIa) and diphasic serovars (IIIb) of the former
subgenus 111. Two other DNA subgroups (V and VI) have
been characterized (21, 23). All seven DNA subgroups can
be identified by using biochemical characteristics (21). The
strict application of the Bacteriological Code (19) led Le
Minor et al. (21, 24) to propose the name of the type species
( S . choleraesuis) for the single Salmonella species and to
propose the following subspecies: S . choleraesuis subsp.
choleraesuis, S . choleraesuis subsp. salamae, S . choleraesuis subsp. arizonae, S . choleraesuis subsp. diarizonae,
S . choleraesuis subsp. houtenae, and S . choleraesuis subsp.
bongori. These six names were validated by announcement
in the International Journal of Systematic Bacteriology (8).
The seventh subspecies, S . choleraesuis subsp. indica, was
recently published and has been validated by announcement
in the International Journal of Systematic Bacteriology (9).
Serovar names would then escape the domain of the Code
(19) and be printed in Roman type (not italics) starting with
a capital letter (e.g., S . choleraesuis subsp. choleraesuis ser.
London).
Need for distinction between the single Salmonella species
name and serotype names. Since the proposal for a single
Salmonella species was made (4, 24), it appeared that the
strict application of the Code (19) would lead to confusion
when the correct names are used in clinical practice. It is
known that different Salmonella serovars can cause different
clinical conditions. Some are causal agents of typhoid fever,
a strictly human disease (e.g., serovars Typhi and Paratyphi
A); others are ubiquitous agents of febrile diarrhea (e.g.,
serovars Typhimurium and Choleraesuis) or cause a strictly
animal disease (e.g., serovars Abortusovis and Gallinarum).
The use of a name such as S . choleraesuis subsp.
choleraesuis serovar Typhi might lead to accidents endangering health or life or both since the pathogenicity of the
ubiquitous serovar Choleraesuis is in the majority of cases
different from that of the strictly human serovar Typhi.
A proposal to emend the Code has recently been published
(27) and accepted (13) and defines a perilous name (nomen
periculosum) as “a name, the application of which is likely
to lead to accidents endangering health or life or both. This
application is restricted to a proposed change in the specific
epithet of a nomenspecies which is widely recognized as
contagious, virulent or highly toxinogenic to that, for example, of a subspecies of a species having a different host range
or degree of contagiousness or virulence.” The name S .
choleraesuis could as well be considered an ambiguous name
(nomen ambiguum, Rule 56a) for the same reasons.
The nomenclature should reflect advances in the taxonomical science. Since taxonomic studies have shown that
Salmonella serovars constitute a single species, microbiologists who accept this one-species concept should use a single
name for the species. Since the name presently applicable to
the single Salmonella species ( S . choleraesuis) is likely to
cause confusion and a health hazard, it should be changed to
a nonconfusing name. 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.
Instead, we request that the Judicial Commission of the
International Committee of Systematic Bacteriology change
the type species of the genus Salmonella. To avoid further
confusion, the name of the single Salmonella species should
not have been (and should never be) that of a serovar.
Proposal for Salmonella enterica sp. nov., nom. rev., for the
type species of the genuq Salmonella. This name proposed in
1952 by Kauffmann and Edwards (14) is already used in the
last edition of Edwards and Ewing’s Identification of Enterobacteriaceae (6). This proposal received unanimous support
from the members of the Subcommittee of Enterobacteriaceae of the International Committee on Systematic
Bacteriology at the XIV International Congress of Microbiology (Manchester, U.K.,1986). Keeping strain ATCC
13312 (type strain of S . choleraesuis) as the type strain of S .
enterica would make S . choleraesuis and S . enterica objective synonyms, which contradict the Code. Thus, we propose that Salmonella enterica be represented by a new type
strain derived from the thoroughly studied strain LT2 (25,
28, 29).
Description of Salmonella enterica sp. nov., nom. rev.
Salmonella enterica (Gr. n. enteron, gut; L. adj. enterica, of
the gut). The description of S . enterica is that of S .
choleraesuis sensu Le Minor et al. (24).
Strains of S . enterica have the following properties typical
of the family Enterobacteriaceae (3). Gram-negative straight
rods, 0.5 to 1.5 by 2.0 to 0.5 pm. Oxidase negative, catalase
positive, reduce nitrate to nitrite, ferment D-glucose, and
grow well on media containing peptone or meat extract.
Usually motile with peritrichous flagella. Nitrate reductase is
of type A (26). Urea not hydrolyzed. Phenylalanine and
tryptophan not deaminated. Lipase and deoxyribonuclease
not produced. Gas usually produced from glucose and H2S
produced from thiosulfate. Tetrathionate reduced to thiosulfate (20), indole not produced, citrate utilized as the sole
carbon source, lysine and ornithine decarboxylated. Acid
not produced from sucrose and adonitol.
The guanine-plus-cytosine content of the DNA is 50 to 53
mol% (7).
In contrast to the other species of the family Enterobacteriaceae most S . enterica strains of subspecies enterica,
salamae, diarizonae, and indica may alternatively express
two different specificities of their flagellar (H) antigen.
Description of the type strain. Strain CIP 60.62T derived
from the wild strain LT2 (H2S producing) was deposited in
the Collection of the Institut Pasteur by M. Demerec in 1960.
LT2 means Lillengen strain type 2 (25). Genetically, it is the
best known Salmonella strain (28, 29). Many mutants have
been isolated from the original strain which is prototrophic.
Some of these mutants are used in tests for detection of
mutagens or carcinogens (1).
Biochemical characteristics of strain LT2 are typical of S .
enterica subsp. enterica (21, 23, 24); acid not produced from
lactose, salicine, and galacturonate; o-nitrophenyl-P-Dgalactopyranoside and malonate tests negative, gelatin not
hydrolyzed, no growth in the presence of KCN. Acid
produced from dulcitol, mucate, and sorbitol; L-( +)-tartrate
test positive. Lysed by phage 01. In addition, this strain
grows on a defined medium with glucose or citrate (Simmons) as sole carbon source. Acid produced from xylose,
arabinose, rhamnose, mannose, mannitol, maltose, trehalose, inositol, and melibiose. Acid not produced from
adonitol, sucrose, raffinose, cellobiose. Lysine and ornithine
decarboxylated, tetrathionate reduced, y-glutamyltransferase produced, indole and P-glucuronidase not produced.
By using specially manufactured API strips (API System,
La Balme les Grottes, France), which contained sole carbon
sources, and by following a method described elsewhere
(P. A. D. Grimont, T. A. Jackson, E. Ageron, and M. J.
Noonan, Int. J. Syst. Bacteriol., in press), we found that the
type strain showed the following nutritional characteristics.
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VOL. 37, 1987
REQUEST FOR AN OPINION
Growth occurred in 4 days on N-acetyl-D-glucosamine,
cis-aconitate, D-alanine, L-alanine, L-arabinose, L-aspartate,
citrate, dulcitol, ethanolamine, D-fructose, L-fucose, fumarate, D-galactose, gentisate, D-gluconate, D-glucosamine, Dglucose, D-glucuronate, L-glutamate, DL-glycerate, glycerol,
meta-hydroxybenzoate, myo-inositol, DL-lactate, L-malate,
maltose, maltotriose, D-mannitol, D-mannose, D-melibiose,
a-methyl-D-galactop yranoside , p-met hyl-D-glucopyranoside, mucate, L-proline, propionate, L-rhamnose, D-ribose,
D-saccharate, L-serke, D-sorbitol, succinate, D-tagatose,
D-tartrate, L-tartrate, meso-tartrate, D-trehalose, tricarballylate, and D-xylose. No growth occurred in 4 days on
trans-aconitate, adonitol, DL-y-aminobutryrate, DL-8aminovalerate, D-arabitol, L-arabitol, benzoate, betaine,
caprate, caprylate, D-cellobiose, m-coumarate, i-erythritol,
esculin, D-galacturonate, P-gentiobiose, glutarate, histamine, para-hydroxybenzoate, DL-P-hydroxybutyrate, 2ketogluconate, a-ketoglutarate, lactose, lactulose, D-lyxose,
malonate, maltitol, D-melezitose, P-methyl-D-galactopyranoside, 3-methylglucose, a-methyl-D-glucopyranoside,
palatinose, phenylacetate, 3-phenylpropionate, protocatechuate, putrescine, quinate, D-raffinose, L-sorbose, sucrose, trigonelline, tryptamine, D-turanose, and xylitol. The
antigenic formula is 4,5,12:i:1,2. Factor 0:l may be expressed after phage conversion (10, 11, 37).
This strain carries a plasmid of about 90 kilobases (31, 32).
Nomenclatural corollary. The following subspecies are
new combinations: S . enterica subsp. enterica comb. nov.
(type strain CIP 60.62), formerly S . choleraesuis subsp.
choleraesuis (with a new type strain); S. enterica subsp.
salamae comb. nov. (type strain NCTC 5773, CIP 8229),
formerly S . choleraesuis subsp. salamae; S . enterica subsp.
arizonae comb. nov. (type strain ATCC 13314, NCTC 8297,
CIP 8230), formerly S . choleraesuis subsp. arizonae; S .
enterica subsp. diarizonae comb. nov. (type strain NCTC
10060, CIP 8231), formerly S . choleraesuis subsp.
diarizonue; S . enterica subsp. houtenae comb. nov. (type
strain CIP 8232), formerly S . choleraesuis subsp. houtenae;
S . enterica subsp. bongori comb. nov. (type strain CIP
8233), formerly S . choleraesuis subsp. bongori, and S .
enterica subsp. indica comb. nov. (type strain CIP 10251),
formerly S . choleraesuis subsp. indica. The nomenclatural
status of the names included in the Approved Lists is thus
modified: S . choleraesuis, S. enteritidis, S . typhi, and S.
typhimurium are subjective synonyms of S . enterica subsp.
enterica. However, if these former names are used, they
should apply only to serovars Choleraesuis, Enteritidis,
Typhi, and Typhimurium, respectively. The former name S .
arizonae, although an objective synonym of S . enterica
subsp. arizonue, had a circumscription which included both
S . enterica subsp. arizonae and S . enterica subsp. diarizonae.
Practical considerations. Clinical, public health or veterinary microbiologists should report Salmonella enterica with
determination of the subspecies and serovar whenever possible. In any case, it is the responsibility of the microbiologist to report in the clearest and most unambiguous way. In
situations where Latin formal nomenclature may not be
clearly understood, a clear, vernacular statement should be
preferred, e.g., Salmonella subsp. I ser. Typhimurium (not
italicized), or even Salmonella Typhimurium (since the
International Congress of Microbiology held in Moscow in
1966, names are only given to new serovars of the first
subspecies). Practical designation of serovars of the other
subspecies may be abbreviated, e.g., Salmonella subsp. I1
followed by the antigenic formula of a serovar of Salmonella
467
enterica subsp. salamae. More detailed examples of clinical
nomenclature of Salmonella serovars are given elsewhere
(23).
ACKNOWLEDGMENT
We thank P. A. D. Grimont for stimulating discussions and the
members of the Subcommittee on Enterobacteriaceae for reading
and approving the first draft of the manuscript.
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