The Genus Citrobacter
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The Genus Citrobacter DIANA BORENSHTEIN AND DAVID B. SCHAUER
Introduction Members of the genus Citrobacter are Gramnegative, nonsporeforming rods belonging to the family Enterobacteriaceae and, as the name suggests, usually utilize citrate as a sole carbon source. These facultative anaerobes typically are motile by means of peritrichous flagella. They ferment glucose and other carbohydrates with the production of acid and gas. They are oxidase negative, catalase and methyl red positive, Voges-Proskauer negative, and do not decarboxylate lysine. Taxonomically, the genus Citrobacter is most closely related to Salmonella and Escherichia. In 1928, Braak described two strains of bacteria capable of forming trimethylene glycol from glycerol under anaerobic conditions. In honor of Freund’s 1881 observation of trimethylene glycol as a fermentation product of glycerol, the strains were designated “Bacterium freundii” (Braak, 1928). One of these strains (ATCC 8454) was among the citrate-utilizing, lactose-fermenting coliforms that Werkman and Gillen designated “Citrobacter freundii” in 1932 (Werkman and Gillen, 1932). This classification was not universally accepted and several synonyms were used to describe these organisms including Escherichia freundii, Colobactrum freundii, Paracolobactrum freundii, Salmonella ballerup, Salmonella hormaechei, the Ballerup group, the Bethesda group, and the Bethesda-Ballerup group. In 1958, the International Subcommittee on the Taxonomy of the Enterobacteriaceae approved the name C. freundii for this heterogeneous group of bacteria. Subsequently, two groups of bacteria that were similar to C. freundii were recognized. The first was designated “C. koseri,” “C. diversus,” or “Levinea malonatica” by different researchers, and the other was designated “L. amalonaticus” (The Genus Citrobacter in the second edition). Eventually, these bacteria were included in the genus Citrobacter, and Frederiksen (1990) requested that the junior synonym C. diversus be formally replaced with C. koseri. In 1993, the Judicial Commission of the International Committee on Systematic Bacteri-
ology granted the request (Joint Commission of the International Committee on Systematic Bacteriology, 1993), and recognized C. koseri as the appropriate name. That same year, Brenner et al. (1993) introduced significant changes to the classification of the genus. Characterization of 112 strains for DNA relatedness using DNA-DNA hybridization resulted in the recognition of 11 distinct Citrobacter species. These groups were called “genomospecies” because the classification was based on DNA relatedness, but the species could also be distinguished by their biochemical profiles. In addition to C. freundii, C. koseri and C. amalonaticus, five new species (C. farmeri, C. youngae, C. braakii, C. werkmanii and C. sedlakii) were identified. The three other species (genomospecies 9, 10 and 11) were later named C. rodentium (Schauer et al., 1995), C. gillenii and C. murliniae (Brenner et al., 1999), respe
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