INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1990, p. 107-108 Vol. 40, No. 1 0020-7713/90/010107-02$02.oo/o Copyright 0 1990, International Union of Microbiological Societies

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.

In 1932 Werkman and Gillen (7) proposed a new genus, taxon C. diversum described by Werkman and Gillen in the Citrobacter, containing seven species. The description of following characteristics: motility, production of H,S, and Citrobacter diversum (sic) of Werkman and Gillen was based production of acid from inositol and raffinose. To this can be on two strains. These strains have not been kept available in added production of acid from glycogen, melizitose, starch, collections, and the name C. diversum did not come into and galactose, as Table 1 shows. general use. Ewing and Davis obviously accepted four deviations to In 1970 Frederiksen (4) described a new species which he lead to the statement about reactions “similar to those named Citrobacter koseri. Among the species described by described by Werkman and Gillen.” However, since it Werkman and Gillen, Frederiksen considered only Citrobac- appears that the new taxon differs by at least another four ter intermedium to be similar to his new group, but as the characteristics from C. diversum as described by Werkman only available strain with this name, Werkman and Gillen and Gillen, it is unlikely that this organism is the same strain M8B (= ATCC 6750), could be shown to be a typical bacterium, and accordingly it should not carry that name. Citrobacter freundii strain, Frederiksen considered his new To use an old name in the old sense in a situation where no taxon a new species not hitherto named. name-bearing strains are kept in collections is also a proce- Similar considerations led Young et al. in 1971 (8) to dure that should not be recommended. After the establish- propose both a new genus, Levinea, and a new species, ment of the Approved Lists of Bacterial Names in 1980 (9, Levinea malonatica, for a new group that they described. such a procedure is no longer possible. An old name can be In 1972 Ewing and Davis (2) published their paper on used only in a new sense, and it is credited to the new Citrobacter diversus, using the specific epithet of Werkman authors and has priority from the new date of valid publica- and Gillen for a group of organisms that they described. tion. Similar strains had been described but not named by Wash- Ewing and Davis stated that “the authors adopted this ington et al. in 1969 (6) and by Booth and MacDonald in 1971 name.” This could imply that they did not intend to use the (1). name C. diversus in the sense of Werkman and Gillen, in The authors involved realized that they were probably which case this name might have been considered a later describing similar strains, as can also be seen when the synonym of C. koseri. However, they used the term “C. descriptions are compared. Representative strains received diversus Werkman and Gillen” and so formally referred the from the authors mentioned above (except Werkman and new taxon to the species described by Werkman and Gillen. Gillen) were examined in my laboratory and were found to be phenotypically alike. There seems to be no doubt among As none of the strains of C. diversum of Werkman and the workers involved that the same species was recognized Gillen were kept, and as the new taxon differs by at least and described independently in five different places at about eight characteristics from C. diversum Werkman and Gillen, the same time. the name C. diversus is incorrectly used for the new taxon. Ewing and Davis (2) reintroduced the epithet diversus for Therefore, I formally request that Citrobacter diversus the new taxon. These authors emphasized the fermentation Werkman and Gillen be placed on the list of nomina re- of adonitol described by Werkman and Gillen for C. diver- jicienda. sum, and the new taxon also ferments adonitol; they “adopt- A decision to place C. diversus on the list of nomina ed this name for these particular bacteria,” that, as they rejicienda will make Citrobacter koseri the valid name for said, “yielded reactions that were similar to those described this taxon, as Levinea malonatica is a later synonym, and by Werkman and Gillen for C. diversum.” As the two strains the problem posed by one organism having three different studied by Werkman and Gillen had not been kept, they names, all on the Approved Lists of Bacterial Names, will be were not included in the study of Ewing and Davis, and the solved. allocation of the new taxon to the species described by It may still be argued that the genus Levinea should be Werkman and Gillen then rests upon reactions “that were maintained; in that case Levinea koseri is a correct combi- similar to those described by Werkman and Gillen for C. nation for the species. diversum. ” The type strain of C. koseri is strain 14804 (= ATCC 27028 The taxon described by Ewing and Davis differed from the = CCM 2537).

107 108 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

H,S pro- H,S pro- Production of acid from: Year of Organism description Reference !:;i:f Motility described by: zt:: method) Glycogen Inositol Melezitose Raffinose Starch Galactose

Werkman and Gillen 1932 7 2 -b + + + + + + - Washington et al. 1969 6 52 98 0 0 Frederiksen 1970 4 30 100 100 (w) (100) (w) Young et al. 1971 8 58 100 0 0 0 Booth and McDonald 1971 1 40 92.5 (2) (100) (100) 0 Ewing and Davis 1972 2 113 93 0 10 0 0 Farmer et al. 1985 3 92 100 0 0 0 Frederiksen' 58 100 100 (w) 0 (86) 0 0 0 100

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 4. Frederiksen, W. 1970. Citrobacter koseri (n.sp.) a new species 1. Booth, E. V., and S. McDonald. 1971. A new group of enterobac- within the genus Citrobacter, with a comment on the taxonomic teria, possibly a new Citrobacter sp. J. Med. Microbiol. 4: position of Citrobacter intermedium (Werkman and Gillen). Publ. 329-336. Fac. Sci. Univ. J. E. Purkyne Brno K47:89-94. 2. Ewing, W. H., and B. R. Davis. 1972. Biochemical characteriza- 5. Skerman, V. B. D., V. McGowan, and P. H. A. Sneath (ed.). 1980. tion of Citrobacter diversus (Burkey) Werkman and Gillen and Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30: designation of the neotype strain. Int. J. Syst. Bacteriol. 22: 225-420. 12-18. 6. Washington, J. A., 11, P. Yu, and W. J. Martin. 1969. Biochem- 3. Farmer, J. J., 111, B. R. Davis, F. W. Hickman-Brenner, A. ical and clinical characteristics and antibiotic susceptibility of McWhorter, G. P. Huntley-Carter, M. A. Asbury, C. Riddle, atypical Enterobacter cloacae. Appl. Microbiol. 17S43-846. H. G. Wathen-Grady, C. Elias, G. R. Fanning, A. G. Steigerwalt, 7. Werkman, C. H., and G. F. Gillen. 1932. Bacteria producing C. M. O'Hara, G. K. Morris, P. B. Smith, and D. J. Brenner. trimethylene glycol. J. Bacteriol. 23:167-182. 1985. Biochemical identification of new species and biogroups of 8. Young, V. M., D. M. Kenton, B. J. Hobbs, and M. R. Moody. Enterobacteriaceae isolated from clinical specimens. J. Clin. 1971. Levinea, a new genus of the family Enterobacteriaceae. Microbiol. 21:46-76. Int. J. Syst. Bacteriol. 21:58-63.