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Yersinia Aldovae (Formerly Yersinia Enterocolitica-Like Group X2): a New Species of Enterobacteriaceae Isolated from Aquatic Ecosystems HERVE BERCOVIER,'T ARNOLD G

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Yersinia Aldovae (Formerly Yersinia Enterocolitica-Like Group X2): a New Species of Enterobacteriaceae Isolated from Aquatic Ecosystems HERVE BERCOVIER,'T ARNOLD G INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1984, p. 166-172 Vol. 34, No. 2 OO20-7713/84/020166-07$02.00/0 Yersinia aldovae (Formerly Yersinia enterocolitica-Like Group X2): a New Species of Enterobacteriaceae Isolated from Aquatic Ecosystems HERVE BERCOVIER,'t ARNOLD G. STEIGERWALT,2 ANNIE GUIYOULE,' GERALDINE HUNTLEY-CARTER,3 AND DON J. BRENNER2* Centre National des Yersinia, fnstitut Pasteur, 15724 Paris, Cedek 15, France,' and Molecular Biology Laboratory, Biotechnology Branch,2 and Enteric Laboratory Section, Enteric Diseases Branch13Division of Bacterial Diseases, Center for Infectious Diseases, Centers for Disease Control, Atlanta, Georgia 30333 Previously, a group of 40 Yersinia enterocolitica-like strains that were isolated from water and fish were called group X2. These strains produced acid from L-rhamnose, did not ferment sorbose, cellobiose, melibiose, or raffinose, and rarely fermented sucrose (5% in 48 h, 10% in 7 days). This pattern of reactions separated group X2 strains from Yersinia enterocolitica, Yersinia intermedia, Yersinia frederiksenii, and Yersinia kristensenii. Positive reactions for acetoin production (Voges-Proskauer test), ornithine decarbox- ylase, and lack of acid production from melibiose distinguished group X2 strains from both Yersinia pseudotuberculosis and Yersinia pestis. Group X2 strains exhibited variable reactions only in tests for citrate utilization, hydrolysis of Tween 80, and acid production from maltose. Genetically, group X2 strains formed a single deoxyribonucleic acid hybridization group with an average level of relatedness of 86% or more (86% as determined by the S1 method at 60°C or by the hydroxyapatite method at 75°C and 92% as determined by the hydroxyapatite method at 60°C). The level of divergence among related sequences in 60°C reactions was 0.5%, as determined by the hydroxyapatite method. The relatedness of group X2 strains to other Yersinia species was 42 to 73% in 60°C reactions. The divergence in these reactions was 11.0 to 15.5%, and the relatedness to other yersiniae in 75°C reactions was 21 to 38%. Group X2 strains were 11 to 32% related to 67 species of the Enterobacteriaceae that belonged to genera other than Yersinia. On the basis of these biochemical and genetic data, we believe that group X2 represents a single new species in the genus Yersinia. The name Yersinia aldovae sp. nov. is proposed for this species. The type strain of Y. aldovae is strain CNY 6005 (= CDC 669-83 = ATCC 35236). Strains that resembled Yersinia enterocolitica but were have all been deposited in the American Type Culture atypical by virtue of acid production from L-rhamnose and Collection, Rockville, Md. All bacteria were cultivated negative reactions for fermentation of sorbose, cellobiose, either at 28°C (most Yersinia strains) or at 36°C and were melibiose, and usually sucrose were described as group X2 maintained on nutrient agar. strains by Bercovier et al. (3). Subsequently, Brenner et al. Cultural and biochemical characteristics. The colonial mor- showed that strain CNY 6005T (T = type strain), represent- phology of Y. aldovae was observed after 2 days of aerobic ing group X2, was substantially related to, but genetically growth at 28°C on petri plates containing nutrient agar. The distinct from, all Yersinia species, as determined by deoxyri- flagella of Y. aldovae strain CNY 6005= were studied by light bonucleic acid (DNA) hybridization (8). microscopy after cells grown overnight at 28°C on semisolid In this report we describe the biochemical characteristics nutrient agar were stained with Rhodes flagellum strain. The and sources of 40 group X2 strains and the levels of DNA biochemical tests were done as previously described (1, 2, relatedness among 28 of these strains. We show that group 12). Unless otherwise stated, the biochemical tests were X2 strains do, in fact, constitute a new species in the genus done at 28°C. Hafnia-specific bacteriophage 1672 of Guinee Yersinia. The name Yersinia aldovae sp. nov. is proposed and Valkenburg was used as described previously (11). for this new species. DNA methods. DNA was isolated by the methods of Brenner et al. and Hickman et al. (7, 13). The guanine-plus- MATERIALS AND METHODS cytosine content of Y.aldovae strain CNY 6005T DNA was Bacterial strains. The 40 Y. aldovae strains which we determined by optical denaturation of high-molecular-weight studied were sent to the Centre National des Yersinia (H. H. DNA diluted in 0.1X SSC (1x SSC is 0.15 M NaCl plus 0.015 Mollaret, Institut Pasteur, Paris, France) from Czechoslova- M sodium citrate) (14). Using the equation of Owen et al. kia and Norway as atypical Y. enterocolitica-like strains. (15), we calculated the base compositions; these were deter- The origins and serological and phage-typing characteristics mined in triplicate, and Escherichia coli B DNA was includ- of these strains are shown in Table 1. The strains represent- ed as a control in each determination (the thermal denatur- ing other Yersinia species and other genera of the Enterobac- ation midpoint of Escherichia coli B DNA in 0.1 X SSC was teriaceae that were used in the DNA hybridization studies 75.5OC). DNAs from Y. aldovae strains CNY 6005= and CNY 7618 were labeled with 32P04in vivo or with 3H in vitro (7, 13). DNA hybridization was done first at 60°C by using * Corresponding author. the S1 endonuclease method and diethylaminoethyl cellulose t Present address: Department of Clinical Microbiology, The filters, as described by Popoff and Coynault (16). In these Hebrew University, Hadassah Medical School, Jerusalem, Israel. experiments DNA from Y. aldovae CNY 6005T was labeled 166 VOL. 34, 1984 YERSZNZA ALDOVAE SP. NOV. 167 TABLE 1. Origins and serological and phage typing characteristics of the 40 Y. aldovae strains studied Laboratory strain no. CNY strain no.a Habitat Countryb Sent by: Serogroup Phage type 1 6005T Drinking water C E. Aldova NT' XO 2 6679 Drinking water C E. Aldova 17 XO 3 7089 Surface water C E. Aldova 17 XO 4 7090 Drinking water C E. Aldova 17 5 7091 Drinking water C E. Aldova 17 6 7092 Drinking water C E. Aldova NT 7 7096 River C E. Aldova NT 8 7109 Water C E. Aldova NT 9 7111 Surface water C E. Aldova 17 10 7112 Surface water C E. Aldova 7,8 11 7328 Drinking water C E. Aldova 798 12 7330 Swimming pool C E. Aldova NT 13 7331 Surface water C E. Aldova NT 14 7332 Surface water C E. Aldova NT 15 7618 Fish N G. Kapperud NT 16 7622 Fish N G. Kapperud NT 17 7632 Fish N G. Kapperud NT 18 7683 Water C E. Aldova 22 19 7898 Water N G. Langeland NT 20 7927 Water N G. Langeland NT 21 7928 Water N G. Langeland NT 22 7970 Water N G. Langeland NT 23 7971 Water N G. Langeland NT 24 8285 Water N G. Langeland 6,31 25 8286 Water N G. Langeland 6,31 26 8287 Water N G. Langeland NT 27 8288 Water N G. Langeland 6,31 28 8290 Water N G. Langeland NT 29 8516 Drinking water C E. Aldova 17 30 8619 Drinking water C E. Aldova NT 31 8626 Drinking water C E. Aldova NT 32 863 1 Drinking water C E. Aldova NT 33 8632 Drinking water C E. Aldova NT 34 8780 Drinking water C E. Aldova 6,30 35 8784 Drinking water C E. Aldova 21 36 8789 Drinking water C E. Aldova NT 37 8790 Drinking water C E. Aldova 17 38 8791 Drinking water C E. Aldova 17 39 8793 Drinking water C E. Aldova 6,30 40 9553 Drinking water C E. Aldova NT a CNY, Centre National des Yersinia (H. H. Mollaret, Institut Pasteur, Paris, France). C, Czechoslovakia; N, Norway. NT, Untypable. in vitro with [3H]thymidine. Subsequently, DNA hybridiza- L-rhamnose, D-xylose, i-inositol, the Voges-Proskauer reac- tion was done by the hydroxyapatite method at 60 and 75"C, tion, Simmons citrate, ornithine decarboxylase, beta-galac- using DNAs from Y. aldovae strains CNY 6005T and CNY tosidase (o-nitrophenyl-P-D-galactopyranoside),and, of 7618 that were labeled with 32P04in vivo. course, motility. These data (except the motility, methyl red, Voges-Proskauer, beta-xylosidase, and Simmons citrate RESULTS data) are not shown for all strains, but the results of the 36 k Phenotypic characteristics, The 40 strains of Y. aldovae 1°C reactions for representative strains CNY 6005T and examined gave mostly homogeneous reactions in biochemi- CNY 7618 are shown in Table 2. cal tests done at 28°C (Table 2). The characteristics common Of the 40 Y. aldovae strains, 17 were typable in slide to all of the strains studied are listed below. A total of 36 agglutination tests for 0 antigens by the scheme of Wauters strains did not ferment sucrose; 2 strains fermented sucrose et al. (19). Eight strains were serogroup 0:17 strains, fol- within 48 h, and 2 strains fermented sucrose after 4 days. lowed by decreasing numbers of strains in serogroups Utilization of citrate (Simmons), acid production from malt- 0:6,31, 0:6,30, 0:7,8, 0:21, and 0:22 (Table 1). All but 1 of ose, and hydrolysis of Tween 80 were independently vari- the 40 strains belonged to either phage type X, or phage type able reactions in the 40 Y. aldovae strains. Two strains were X,; these phage types consist of bacteriophages that are nonmotile at 28"C, and two other strains gave negative isolated from sewage, not of specific temperate bacterio- reactions for urease. A single strain gave a negative test for i- phages that are isolated from Y. enterocolitica (Table 1). inositol. Like other Yersinia species, especially the L-rham- Genetic characteristics.
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