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Current system of Salmonella nomenclature

used by WHO, CDC, and ASM

 Lin-Hui Su and Cheng-Hsun Chiu

              Salmonella is named after an American bacteriologist, D. E. Salmon, who first isolated Salmonella choleraesuis from porcine intestine in 1884 (1). Salmonellae are a group of bacterial organisms with a high genetic similarity and are differentiated by their serotyping results. The antigenic classification system of various Salmonella serotypes used today is a result accumulated from many years of studies on antibody interactions with surface antigens of Salmonella organisms established by Kauffman and White almost a century ago. All antigenic formulae of recognized Salmonella serotypes are listed in a document called the Kauffmann-White scheme (2). The World Health Organization Collaborating Centre for Reference and Research on Salmonella at the Pasteur Institute, Paris, France (WHO Collaborating Centre) is responsible for the updating of the scheme. Every year newly recognized serotypes are reported in the Research in Microbiology by Popoff et al. and in the latest report published in 2004, there are a total of 2,541 serotypes in the genus Salmonella (3). The terms “serotype” and “serovar” are both frequently used, but according to the Rules of the Bacteriological Code (1990 Revision) established by the Judicial Commission of the International Committee on the Systematics of Prokaryotes, the term serovar is preferred to the term serotype. Thus “serovar” is used in the Kauffmann-White scheme.

              Salmonella nomenclature is complex and still evolving. Currently, the nomenclature system used at the Centers for Disease Control and Prevention (CDC) for the genus Salmonella is based on recommendations from the WHO Collaborating Centre. According to the CDC system, the genus Salmonella contains two species, S. enterica, the type species, and S. bongori. On March 18, 2005, a new species, “Salmonella subterranean” was validly approved by the Judicial Commission (4); CDC may incorporate the species in their system in the near future. S. enterica consists of six subspecies (2,5): I, S. enterica subsp. enterica; II, S. enterica subsp. salamae; IIIa, S. enterica subsp. arizonae; IIIb, S. enterica subsp. diarizonae; IV, S. enterica subsp. houtenae; and VI, S. enterica subsp. indica.

              In subspecies I, serotypes (or serovars) are designated by a name usually indicative of the associated diseases, their geographic origins, or their usual habitats. In the remaining subspecies as well as those of S. bongore, antigenic formulae determined according to the Kauffmann-White scheme (2) are used for those unnamed serotypes. Some members of these subspecies may have been named before 1966 and thus their names are retained and cited as those in the subspecies I.

              To avoid confusion between serotypes and species, the serotype name is not italicized and starts with a capital letter. When cited at the first time in a report, the genus name is given followed by the word “serotype” (or the abbreviation “ser.”) and then the serotype name, e.g., Salmonella serotype or ser. Choleraesuis, and Salmonella serotype or ser. Typhi. Afterward the name may be shortened with the genus name followed directly by the serotype name, e.g., Salmonella Choleraesuis or S. Choleraesuis, and Salmonella Typhi or S. Typhi (3). Because the type species name, enterica, has not been approved before 2005, serotype names are used directly after the genus name without the mention of the species. Following the officially approval of “enterica” as the type species name from January 2005 (6), further amendment to include species name in the Salmonella nomenclature by CDC may be expected.

              For those designated by their antigenic formulae, the subspecies name is written in Roman letters (not italicized) followed by their antigenic formulae, including O (somatic) antigens, H (flagellar) antigens (phase 1), and H antigens (phase 2, if present). A colon is used in between each antigen, e.g., Salmonella serotype II 39:z₁₀: z₆. For serotypes in S. bongori (previously belongs to subgenous V), V is still used for consistency, e.g., S. V 13,22:z₃₅:- (3).

              In publications of the American Society for Microbiology (ASM), the Salmonella nomenclature used at CDC was accepted as the standard form by the Publications Board in the 1999 meeting and the Instruction to Authors has been updated to include this information since 2000 (7). The 2006 ASM Instruction to Authors indicated that, for the species, “Salmonella enterica” is used at the first time, and “S. enterica” thereafter; for the subspecies, “Salmonella enterica subsp. arizonae” is used at first, and “S. enterica subsp. arizonae” thereafter. Serotype names should be in Roman type with the first letter capitalized, e.g., Salmonella enterica serotype Typhimurium. After the first use, the serotype may be used without a species name, e.g., Salmonella serotype Typhimurium.

REFERENCES

1. Smith T. The hog-cholera group of bacteria. U.S. Bur Anim Ind Bull 1894; 6:6-40.

2. Popoff MY, Le Minor L. Antigenic formulas of the Salmonella serovars, 8th revision, World Health Organization Collaborating Centre for Reference and Research on Salmonella, Pasteur Institute, Paris, France. 2001.

3. Popoff MY, Bockemühl J, Gheesling LL. Supplement 2002 (no. 46) to the Kauffmann-White scheme. Res Microbiol 2004; 155:568-570.

4. Shelobolina ES, Sullivan SA, O'neill KR, Nevin KP, Lovley DR. Isolation, characterization, and U(VI)-reducing potential of a facultatively anaerobic, acid-resistant bacterium from low-pH, nitrate- and U(VI)-contaminated subsurface sediment and description of Salmonella subterranea sp. nov. Appl Environ Microbiol 2004; 70:2959-2965.

5. Brenner FW, McWhorter-Murlin AC. Identification and serotyping of Salmonella. Centers for Disease Control and Prevention, Atlanta, Ga. 1998.

6. Judicial Commission of the International Committee on Systematics of Prokaryotes. The type species of the genus Salmonella Lignieres 1900 is Salmonella enterica (ex Kauffmann and Edwards 1952) Le Minor and Popoff 1987, with the type strain LT2T, and conservation of the epithet enterica in Salmonella enterica over all earlier epithets that may be applied to this species. Opinion 80. Int J Syst Evol Microbiol 2005; 55:519-520.

7. Publications Board. Publications Board meeting minutes. Salmonella nomenclature. ASM News 1999; 65:769.