INTERNATIONAL
JOURNAL OF SYSTEMATIC
BACTERIOLOGY,
Jan. 1990, p. 107-108
0020-7713/90/010107-02$02.oo/o
Copyright 0 1990, International Union of Microbiological Societies
Vol. 40, No. 1
Correct Names of the Species Citrobacter koseri, Levinea
malonatica , and Citrobacter diversus
Request for an Opinion
WILHELM FREDERIKSEN
Department of Diagnostic Bacteriology and Antibiotics, Statens Seruminstitut, DK-2300 Copenhagen S,Denmark
The single species carrying the three names Citrobacter koseri, Levinea malonatica, and Citrobacter diversus
differs by at least eight characteristics from Citrobacter diversum as described by Werkman and Gillen in 1932.
It is obviously not the same organism. Accordingly, the species should not carry the name proposed by
Werkman and Gillen. I request that the name Citrobacter diversus be placed on the list of nomina rejicienda.
Citrobacter koseri is the correct name. Levinea koseri is a correct combination when the genus Levinea is
accepted. The epithet maZoonatica is a later synonym of the epithet koseri.
taxon C. diversum described by Werkman and Gillen in the
following characteristics: motility, production of H,S, and
production of acid from inositol and raffinose. To this can be
added production of acid from glycogen, melizitose, starch,
and galactose, as Table 1 shows.
Ewing and Davis obviously accepted four deviations to
lead to the statement about reactions “similar to those
described by Werkman and Gillen.” However, since it
appears that the new taxon differs by at least another four
characteristics from C. diversum as described by Werkman
and Gillen, it is unlikely that this organism is the same
bacterium, and accordingly it should not carry that name.
To use an old name in the old sense in a situation where no
name-bearing strains are kept in collections is also a procedure that should not be recommended. After the establishment of the Approved Lists of Bacterial Names in 1980 (9,
such a procedure is no longer possible. An old name can be
used only in a new sense, and it is credited to the new
authors and has priority from the new date of valid publication.
Ewing and Davis stated that “the authors adopted this
name.” This could imply that they did not intend to use the
name C. diversus in the sense of Werkman and Gillen, in
which case this name might have been considered a later
synonym of C. koseri. However, they used the term “C.
diversus Werkman and Gillen” and so formally referred the
new taxon to the species described by Werkman and Gillen.
As none of the strains of C. diversum of Werkman and
Gillen were kept, and as the new taxon differs by at least
eight characteristics from C . diversum Werkman and Gillen,
the name C. diversus is incorrectly used for the new taxon.
Therefore, I formally request that Citrobacter diversus
Werkman and Gillen be placed on the list of nomina rejicienda.
A decision to place C. diversus on the list of nomina
rejicienda will make Citrobacter koseri the valid name for
this taxon, as Levinea malonatica is a later synonym, and
the problem posed by one organism having three different
names, all on the Approved Lists of Bacterial Names, will be
solved.
It may still be argued that the genus Levinea should be
maintained; in that case Levinea koseri is a correct combination for the species.
The type strain of C. koseri is strain 14804 (= ATCC 27028
= CCM 2537).
In 1932 Werkman and Gillen (7) proposed a new genus,
Citrobacter, containing seven species. The description of
Citrobacter diversum (sic) of Werkman and Gillen was based
on two strains. These strains have not been kept available in
collections, and the name C . diversum did not come into
general use.
In 1970 Frederiksen (4) described a new species which he
named Citrobacter koseri. Among the species described by
Werkman and Gillen, Frederiksen considered only Citrobacter intermedium to be similar to his new group, but as the
only available strain with this name, Werkman and Gillen
strain M8B (= ATCC 6750), could be shown to be a typical
Citrobacter freundii strain, Frederiksen considered his new
taxon a new species not hitherto named.
Similar considerations led Young et al. in 1971 (8) to
propose both a new genus, Levinea, and a new species,
Levinea malonatica, for a new group that they described.
In 1972 Ewing and Davis (2) published their paper on
Citrobacter diversus, using the specific epithet of Werkman
and Gillen for a group of organisms that they described.
Similar strains had been described but not named by Washington et al. in 1969 (6) and by Booth and MacDonald in 1971
(1).
The authors involved realized that they were probably
describing similar strains, as can also be seen when the
descriptions are compared. Representative strains received
from the authors mentioned above (except Werkman and
Gillen) were examined in my laboratory and were found to
be phenotypically alike. There seems to be no doubt among
the workers involved that the same species was recognized
and described independently in five different places at about
the same time.
Ewing and Davis (2) reintroduced the epithet diversus for
the new taxon. These authors emphasized the fermentation
of adonitol described by Werkman and Gillen for C. diversum, and the new taxon also ferments adonitol; they “adopted this name for these particular bacteria,” that, as they
said, “yielded reactions that were similar to those described
by Werkman and Gillen for C. diversum.” As the two strains
studied by Werkman and Gillen had not been kept, they
were not included in the study of Ewing and Davis, and the
allocation of the new taxon to the species described by
Werkman and Gillen then rests upon reactions “that were
similar to those described by Werkman and Gillen for C.
diversum.
The taxon described by Ewing and Davis differed from the
”
107
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108
REQUEST FOR AN OPINION
INT. J. SYST.BACTERIOL.
TABLE 1. Characteristics that differentiate C. diversum Werkman and Gillen from the species described by several authors
Organism
described by:
Werkman and Gillen
Washington et al.
Frederiksen
Young et al.
Booth and McDonald
Ewing and Davis
Farmer et al.
Frederiksen'
Year of
description
Motility
method)
1932
1969
1970
1971
1971
1972
1985
zt:
H,S pro- H,S proReferencef:i;:!
7
6
4
8
1
2
3
2
52
30
58
40
113
92
58
+
-b
98
100
100
92.5
93
100
100
Production of acid from:
Glycogen Inositol Melezitose Raffinose Starch Galactose
+
+
+
0
100 (w)
0
(2)
0
0
+
+
-
0
100
0
(100)
10
100 (w)
0
(100) (w)
0
(100)
0
0
(86)
0
0
0
0
0
0
a Iron detection methods other than the TSI method were used to detect H2S production. Werkman and Gillen did not describe the method which they used
for H,S detection.
+, Positive reaction; -, negative reaction. The numbers are the percentages of strains which had positive reactions. The numbers in parentheses are the
percentages of strains which had late positive reactions. (w), Weak positive reaction.
In 1971 through 1973 I examined 42 of my own strains, as well as 4 strains each from Washington, Young, McDonald, and Ewing.
LITERATURE CITED
1. Booth, E. V., and S. McDonald. 1971. A new group of enterobacteria, possibly a new Citrobacter sp. J. Med. Microbiol. 4:
329-336.
2. Ewing, W. H., and B. R. Davis. 1972. Biochemical characterization of Citrobacter diversus (Burkey) Werkman and Gillen and
designation of the neotype strain. Int. J. Syst. Bacteriol. 22:
12-18.
3. Farmer, J. J., 111, B. R. Davis, F. W. Hickman-Brenner, A.
McWhorter, G. P. Huntley-Carter, M. A. Asbury, C. Riddle,
H. G. Wathen-Grady, C. Elias, G. R. Fanning, A. G. Steigerwalt,
C. M. O'Hara, G. K. Morris, P. B. Smith, and D. J. Brenner.
1985. Biochemical identification of new species and biogroups of
Enterobacteriaceae isolated from clinical specimens. J. Clin.
Microbiol. 21:46-76.
4. Frederiksen, W. 1970. Citrobacter koseri (n.sp.) a new species
within the genus Citrobacter, with a comment on the taxonomic
position of Citrobacter intermedium (Werkman and Gillen). Publ.
Fac. Sci. Univ. J. E. Purkyne Brno K47:89-94.
5 . Skerman, V. B. D., V. McGowan, and P. H. A. Sneath (ed.). 1980.
Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30:
225-420.
6. Washington, J. A., 11, P. Yu, and W. J. Martin. 1969. Biochemical and clinical characteristics and antibiotic susceptibility of
atypical Enterobacter cloacae. Appl. Microbiol. 17S43-846.
7. Werkman, C. H., and G. F. Gillen. 1932. Bacteria producing
trimethylene glycol. J. Bacteriol. 23:167-182.
8. Young, V. M., D. M. Kenton, B. J. Hobbs, and M. R. Moody.
1971. Levinea, a new genus of the family Enterobacteriaceae.
Int. J. Syst. Bacteriol. 21:58-63.
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