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Taxonomic Dissection of the Streptococcus Bovis Group By International Journal of Systematic and Evolutionary Microbiology (2002), 52, 1247–1255 DOI: 10.1099/ijs.0.02044-0 Taxonomic dissection of the Streptococcus bovis group by analysis of manganese- dependent superoxide dismutase gene (sodA) sequences: reclassification of ‘Streptococcus infantarius subsp. coli’asStreptococcus lutetiensis sp. nov. and of Streptococcus bovis biotype II.2 as Streptococcus pasteurianus sp. nov. Laboratoire Mixte Pasteur- Claire Poyart, Gilles Quesne and Patrick Trieu-Cuot Necker de Recherche sur les Streptocoques et Streptococcies and Unite! Author for correspondence: INSERM 411, Faculte! de Claire Poyart. Tel: j33 (1) 40 61 56 79. Fax: j33 (1) 40 61 55 92. Me! decine Necker-Enfants e-mail: cpoyart!pasteur.fr Malades, 75730 Paris Cedex 15, France The taxonomic dissection of the Streptococcus bovis–Streptococcus equinus group was carried out upon obtaining sequences for the manganese-dependent superoxide dismutase gene (sodA) of the type strains of S. bovis, Streptococcus caprinus, S. equinus, Streptococcus gallolyticus, Streptococcus infantarius, Streptococcus macedonicus and Streptococcus waius. The sodA sequences of 29 streptococcal strains of animal and human origin that were related to S. bovis were also sequenced. A phylogenetic analysis of the sodA sequences revealed that the S. bovis–S. equinus group comprises five different clusters that correspond to five distinct species. The type strains of S. bovis and S. equinus were associated in the same cluster, corresponding to the species S. equinus. The type strains of S. caprinus, S. gallolyticus, S. macedonicus and S. waius were associated in the same cluster, which defined a single species containing S. gallolyticus and its junior synonym S. caprinus, and S. macedonicus and its junior synonym S. waius. The two subspecies thought to constitute the species S. infantarius, namely S. infantarius subsp. infantarius and ‘S. infantarius subsp. coli’, were located in two distinct clusters. One of these clusters defined the species S. infantarius and included the type strain of S. infantarius subsp. infantarius. The other cluster defined ‘S. infantarius subsp. coli’, leading to the proposal of its reclassification as the novel species Streptococcus lutetiensis (NEM 782T l CIP 106849T). The remaining cluster comprised all of the strains previously identified as belonging to S. bovis biotype II.2, leading to the proposal to reassign these strains to the novel species Streptococcus pasteurianus (NEM 1202T l CIP 107122T). The results of the phylogenetic analysis were confirmed by DNA–DNA hybridization experiments, thus demonstrating that sequence databases of defined DNA targets, such as sodA, may constitute a valuable alternative approach for modern bacterial systematics. Keywords: Streptococcus bovis, Streptococus lutetiensis sp. nov., Streptococcus pasteurianus sp. nov., superoxide dismutase gene (sodA), 16S rRNA gene ................................................................................................................................................................................................................................................................................................................. Published online ahead of print on 29 November 2001 as DOI 10.1099/ijs.0.02044-0. Abbreviation: sodAint, internal fragment of sodA. The GenBank accession numbers for the sodAint sequences reported in this study can be found in Table 1. The GenBank accession numbers for the 16S rDNA sequences of S. lutetiensis NEM 782T and S. pasteurianus NEM 1202T are AJ297189 and AJ297195, respectively. 02044 # 2002 IUMS Printed in Great Britain 1247 C. Poyart, G. Quesne and P. Trieu-Cuot INTRODUCTION infantarius)to99n8% (S. bovis and S. infantarius). To differentiate such strains, it is possible to use alternative Streptococcus bovis is a normal inhabitant of the single-copy target sequences that exhibit greater se- ruminant and human gut. In humans, it has been quence divergence than that of 16S rDNA. The sodA reported to be the causative agent of meningitis, gene of the Gram-positive cocci, which encodes the septicaemia and endocarditis, and numerous reports manganese-dependent superoxide dismutase (Mn- have suggested a potential relationship between in- SOD), fulfils these criteria. We have previously de- creased faecal carrier levels of S. bovis and human scribed a PCR assay, based on the utilization of gastrointestinal disease (Duval et al., 2001; Grant et degenerate primers, which enabled the amplification of al., 2000; Manfredi et al., 1999; Zarkin et al., 1990). an internal fragment representing approximately 83% Therefore, the correct identification of S. bovis isolates of the sodA gene encoding Mn-SOD in various Gram- is important in clinical microbiology laboratories. positive bacteria, including streptococci and entero- The taxonomic status of S. bovis strains has been cocci (Poyart et al., 1995). We have also reported that evolving in the last few decades and has progressively sequencing the sodA PCR product, with the same changed according to the description of new species degenerate primers, constitutes a valuable approach to originally identified as S. bovis. In the 1990s, four new the genotypic identification of species belonging to the species were described, Streptococcus gallolyticus genera Streptococcus and Enterococcus (Poyart et al., (Osawa et al., 1995), Streptococcus macedonicus (Tsak- 1995, 1998, 2000). This target gene has also been used alidou et al., 1998), Streptococcus waius (Flint et al., for the identification of other bacteria at the species 1999) and Streptococcus infantarius (Bouvet et al., level, including coagulase-negative staphylococci 1997). In clinical laboratories, the accurate identifica- (Poyart et al., 2001) and mycobacteria (Zolg & tion of these streptococci is based on phenotypic Philippi-Schulz, 1994). In this work, we carried out a characteristics that permit the classification of S. bovis taxonomic analysis of the S. bovis group, by using the strains into two biotypes (Facklam et al., 1984; Knight same approach as described previously and demon- & Schlaes, 1985; Ruoff et al., 1984, 1989). However, strated the usefulness of a sodA-based database for the these phenotypic characterizations are impaired due to species identification of strains belonging to the S. the variable expression of certain traits and because of bovis–S. equinus complex. Furthermore, phylogenetic the frequent ambiguity in the interpretation of such studies of sodA gene sequences and DNA–DNA data. Consequently, nucleic-acid-based technologies, hybridization experiments support the recognition of such as DNA–DNA hybridization or the amplification two distinct novel species within the genus Strep- of selected targets, have been developed to complement tococcus, for which the names Streptococcus lutetiensis and improve the identification of streptococci at the (formerly ‘S. infantarius subsp. coli’) and Streptococcus species level (Garnier et al., 1997; Kawamura et al., pasteurianus (formerly S. bovis biotype II.2) are pro- 1995, 1999; Poyart et al., 1998). Farrow et al. (1984) posed. demonstrated that on the basis of DNA–DNA hybridi- zation data S. bovis strains could be classified into six METHODS genomic groups that exhibited between 40 and 60% DNA similarity with each other. These authors also Bacterial strains and culture conditions. The main charac- demonstrated that biotype I strains were genotypically teristics of the strains used in this study, including the type homogeneous and distinct from biotype II strains, strains, are listed in Table 1. The isolates of S. bovis were of which include the type strains of S. bovis and Strep- various origins and were collected over a period of at least 10 years. All strains were grown at 37 mC on Columbia horse tococcus equinus. More recently, based on 16S rDNA blood agar (bioMe! rieux) or in brain-heart infusion (BHI) sequence analysis, Clarridge et al. (2001) have sug- broth under anaerobic conditions. Cultures were stored at gested that S. bovis biotype II.2 strains constitute a k80 mC in BHI broth (Difco) supplemented with 10% (w\v) separate genospecies that is distinct from S. bovis, S. glycerol until required. gallolyticus and S. infantarius. Phenotypic characteristics. The strains were characterized The interpretation of 16S rDNA sequence data may be for their morphological, growth and biochemical properties. complicated by the fact that divergent 16S rDNA The production of acetoin, enzymic reactions and fermen- sequences may exist within a single organism (Ueda et tation of carbohydrates were determined using the API 20Strep and Rapid ID 32Strep systems, according to the al., 1999) or, alternatively, by the fact that closely manufacturer’s recommendations (bioMe! rieux). All strains related species may have nearly identical 16S rDNA were tested for growth on agar plates supplemented with sequences (Fox et al., 1992). The latter has been shown 40% bile\aesculin, 5% sucrose or 0n04% sodium tellurite. for members of the genus Streptococcus, namely Growth was tested in broth containing 6n5% (w\v) NaCl Streptococcus pneumoniae, Streptococcus mitis and and gas production was assayed in MRS broth (Bio-Rad). Streptococcus oralis (Kawamura et al., 1995). The 16S The presence of the Lancefield’s group D antigen was rDNA sequences of the type strains of the S.bovis determined with the Streptex test, according to the manu- group (S. bovis, Streptococcus caprinus, S. equinus, S. facturer’s recommendations (bioMe! rieux).
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