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Numerical Taxonomy of Yersinia Enterocozitica and Yersinia Enterocozztica-Like Bacteria

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Numerical Taxonomy of Yersinia Enterocozitica and Yersinia Enterocozztica-Like Bacteria INTERNATIONAL JOURNALOF SYSTEMATIC BACTERIOLOGY, OCt. 1981, p. 401-419 Vol. 31, No. 4 0020-77 13/8 1/040401- 19$02.00/0 Numerical Taxonomy of Yersinia enterocozitica and Yersinia enterocoZztica-Like Bacteria GEORG KAPPERUD,’. TOM BERGAN,3 AND J0RGEN LASSEN4 Zoological Institute, University of Oslo,’ Norwegian Defense Microbiological Laboratory,’ Department of Microbiology, Institute of Pharmacy, University of Oslo,’ and National Institute of Public He~lth,~ Oslo, Norway We studied the taxonomic interrelationships of 332 Yersinia strains by using a numerical analysis that was based on 46 cultural and biochemical characters and involved both a hierarchical clustering procedure and a principal components analysis. Yersinia pseudotuberculosis and Yersinia kristensenii were recognized as relatively distinct phenotypic clusters. Y. kristensenii was further distinguish- able from the remaining taxa by antigenic and enterotoxigenic parameters. These results supported the suggestion that Y. kristensenii deserves species status. On the other hand, Yersinia enterocolitica sensu stricto, Yersinia frederiksenii, and Yersinia intermedia constituted a phenotypic continuum. Each of these three taxa prevailed in different parts of a heterogeneous cluster of strains that were connected by intermediate phenotypes. This pattern of overlapping phenotypes was supported further by antigenic properties, habitat preferences, and pathogenic characteristics. Thus, we failed to find a basis for separating Y. enterocolitica sensu stricto, Y. frederiksenii, and Y. intermedia on phenetic, ecological, or pathogenic grounds. We suggest that the taxonomic relationships among these nomenspecies may require further evaluation. Two phenetic clusters contained strains not ascribable to any presently defined species. One of these clusters consisted mainly of rhamnose-positive, sucrdse-negative strains and the other contained strains negative for sucrose or ornithine decarboxylase or both. In Bergey ’s Manual of Determinative Bacte- nomenclature), based on indole production. riology, 8th ed. (12),the genus Yersinia is placed Jantzen and Lassen (18) examined the fatty acid in the family Entero bacteriaceae and contains compositions of Y. enterocolitica and Y. enter- three recognized species, Yersinia pestis, Yer- ocolitica-like bacteria. The genetic, cultural, and sinia pseudotu berculosis, and Yersinia enter- biochemical heterogeneity was not reflected by ocolitica. Two additional species, Yersinia phi- these fatty acid compositions. This is in accord lomiragia (19) and Yersinia ruckeri (15), have with the observations of Bercovier and Carlier been proposed, but these species have not been (3) and Sandhu et al. (K. K. Sandhu, E. J. accepted generally. Bottone, and M. A. Paisano, Abstr. Annu. Meet. Y. enterocolitica as currently recognized is Am. SOC.Microbiol. 1980, 154, p. 93). The data quite heterogeneous, both phenotypically and per se do not suggest a subdivision of Y. enter- genetically. A broad diversity of strains are pres- ocolitica as currently recognized. ently placed in this species. The need for a Brenner (8) and Brenner et al. (10) considered taxonomic revision with a more precise delinea- genetic data obtained by deoxyribonucleic acid tion of Y.enterocolitica has been recognized (6, (DNA)-DNA hybridizations of Yersinia strains. 8, 10, 16, 21, 24, 27, 33, 34, 36, 39, 42, 43). The These workers distinguished three DNA relat- designation Y. enterocolitica-like bacteria has edness groups among Y. enterocolitica and re- been applied to atypical variants. lated bacteria, and from the biochemical prop- In 1973, Knapp and Thal (27) expressed the erties they defined a fourth entity. All groups opinion that the biochemical diversity of the were referred to the genus Yersinia, but only strains designated Y. enterocozitica is sufficient one deserved the name Y.enterocolitica. On the to justify the establishment of two separate spe- other hand, the genetic data of Moore and Bru- cies, Y. enterocolitica and “ Yersinia enteriti- baker (34) have suggested that the relationship dis” (names in quotation marks are not on the of Y. enterocolitica to the genus Yersinia might Approved Lists of Bacterial Names [37] and require further evaluation. Just recently, Ber- have not been validly published since January covier et al. (2, 4), Brenner et al. (9, ll), and 1, 1980; hence, they are without standing in Ursing et al. (40) described comprehensive stud- 40 1 402 KAPPERUD, BERGAN, AND LASSEN INT. J. SYST.BACTERIOL. ies of 175 Y. enterocolitica and related strains. MATERIALS AND METHODS These authors proposed the following four spe- Bacterial strains. We selected 332 strains belong- cies, corresponding to distinct DNA relatedness ing to the genus Yersinia for this study (Table 1). groups: Y. enterocolitica sensu stricto (typical These strains were a priori referred to the following isolates), Yersinia frederiksenii (strains produc- categories of Brenner et al. (11). ing acid from rhamnose), Yersinia intermedia (i) Y. enterocoliticu sensu stricto. A total of 148 (strains producing acid from rhamnose and mel- strains were typical Y. enterocolitica isolates. All pro- duced acid from sucrose but not from melibiose or ibiose), and Yersinia kristensenii (strains not rhamnose. Seven strains belonging to serogroup 3, producing acid from sucrose). biovar 4 (41) were isolated from feces of human pa- One important question that needs to be an- tients with gastroenteritis in Norway (strains 32 swered is how phenotypic differentiation corre- through 38), and 119 strains were isolated from envi- lates with genetic subdivision. The numerical ronmental sources in Scandinavian terrestrial and taxonomy study of Sakazaki et al. (36), which freshwater ecosystems (20, 21, 24, 25, 28, 29) (strains involved the simple matching coefficient and 39 through 157). The remaining 22 strains were re- single-linkageclustering, distinguished four phe- ceived as reference strains from the Pasteur Institute, notypic clusters, three of which corresponded Paris, France (strains 1 through 3, 5 through 15, 20, 21,25 through 29, and 31). approximately to the three different DNA relat- (ii) Y. entenwoliticu-likebacteria. A total of 165 edness groups described by Brenner et al. (10). strains isolated from Scandinavian environmental However, this clustering procedure is known to sources (20, 21, 24, 25) deviated from the pattern of be less discriminating. Harvey and Pickett (16) determinative characteristics typical of Y. enterocolit- examined 190 strains by using the simple match- ica. These were 51 Y.kristensenii strains that did not ing coefficient and clustering by unweighted pair produce acid from sucrose (strains 158 through 208), group analysis. These authors concluded that 55 Y. fiederiksenii strains that produced acid from the numerical taxonomy relationships did not rhamnose (strains 209 through 263), 25 Y. intermedia correlate highly with the results of DNA hybrid- strains that produced acid from rhamnose and meli- izations between strains selected from their phe- biose (strains 264 through 288), and 34 strains which could not be ascribed to any defined species (strains netic clusters. Actually, three strains, including 289 through 322). In addition, five reference strains the centrostrain, were selected from each of the received from the Pasteur Institute, Paris, were clas- main clusters. Two of these did show a good sified as members of Y. kristensenii (strains 16 correlation between genetic classification and through 19 and 30), and four were classified as Y. phenetic classification (namely, the centrostrain frederiksenii (strains 4 and 22 through 24). and one strain phenetically highly related to the (iii) Y. pseudotuberculosis. Seven reference centrostrain). The converse was true for strains strains representing Y.pseudotuberculosis serogroups distantly related to the centrostrain. This is not I through V were received from S. Winblad, Malmo, unexpected, however, since hierarchical numer- Sweden (strains 323 through 329). ical procedures do result in more heterogenous (iv) Y. pseudotuberculosis-likebacteria. Three strains isolated from wild, small mammals in Denmark clusters above certain similarity levels as the (21) exhibited biochemical properties consistent with number of units to be grouped is increased. The the properties of Y.pseudotuberculosis, but they were validity of groups formed by hierarchical clus- antigenically atypical (strains 330 through 332). tering procedures may be assessed by parallel All strains were maintained as stab cultures on meat application of several numerical grouping pro- extract agar at 4°C. cedures. One efficient method which is supple- Cultural and biochemical determinants. For mentary to hierarchical clustering procedures is each strain, 46 cultural and biochemical properties principal components analysis. This method were determined. Incubation was at 37°C unless other- wise stated. The tests were read daily for 4 days. projects the elements to be classified on two- Weakly positive or ambiguous tests were incubated dimensional coordinate plots based on an en- further and were read for 7 days. tirely different computational strategy than Acid from carbohydrates. Acidification of car- phenogram-generating procedures. bohydrate-containing media was studied in liquid me- The aims of this study were (i) to study the dia containing 0.5% carbohydrate in 1%peptone water taxonomic interrelationships of Y.enterocolitica and 0.0025% bromothymol blue as an indicator. The
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