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1 Institut für Mikrobiologie und Genetik, Universität Wien, A-1030 Wien, Austria
2 DSMZ – Deutsche Sammlung für Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
3 Institut für Genetik und Allgemeine Biologie, Universität Salzburg, A-5020 Salzburg, Austria
4 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, A-1210 Wien, Austria
Correspondence
Hans-Jürgen Busse
Hans-Juergen.Busse{at}vu-wien.ac.at
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with meso-diaminopimelic acid as the diagnostic cell-wall diamino acid and an interpeptide bridge of D-asp-D-Glu. The isolate contained menaquinone MK-7 (88 %) as the major component of the quinone system and minor amounts of menaquinone MK-8 (9 %) and menaquinone MK-6 (3 %). The polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, unidentified glycolipids and unidentified phospholipids. The fatty acid profile contained predominantly anteiso-C15 : 0 and significant amounts of iso-C16 : 0, iso-C14 : 0, anteiso-C17 : 0 and C19 : 0. The polyamine pattern consisted of spermine and spermidine as the major compounds. Genomic fingerprints clearly distinguished strain C3H-21T from other Brachybacterium species. The isolate shared the highest 16S rDNA sequence similarities with members of the genus Brachybacterium, in particular Brachybacterium sacelli LMG 20345T, Brachybacterium nesterenkovii DSM 9573T, Brachybacterium rhamnosum LMG 19848T, Brachybacterium alimentarium CNRZ 925T and Brachybacterium fresconis LMG 20336T (97·8–97·2 %). The results of biochemical/physiological characterization, chemotaxonomic characteristics and REP-PCR-generated fingerprints demonstrated that the isolate represents a novel species of the genus Brachybacterium, for which the name Brachybacterium muris (type strain C3H-21T=DSM 14560T=CCM 7047T) is proposed.
Published online ahead of print on 6 June 2003 as DOI 10.1099/ijs.0.02728-0.
The EMBL accession number for the 16S rDNA sequence of Brachybacterium muris C3H-21T is AJ537574.
An image showing the REP-PCR fingerprints of B. muris C3H-21T and related Brachybacterium spp. is available in IJSEM Online.
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). On the basis of serological and molecular biological methods, the presence of other bacterial taxa in the livers of mice has also been detected, including lactobacilli (de Waard et al., 2003) and propionibacteria (Tsuji et al., 1997; Sakao et al., 1999), but nothing is known about their pathogenicity. In the course of our study, we isolated a strain (C3H-21T) from the liver of a laboratory mouse which was preliminarily identified as a member of the genus Brachybacterium. Since the liver of mice is an unusual source for isolation of Brachybacterium, we subjected strain C3H-21T to a detailed taxonomic characterization. For comparison, Brachybacterium faecium CCM 4372T (Collins et al., 1988), Brachybacterium conglomeratum CCM 2589T, Brachybacterium rhamnosum DSM 10240T (Takeuchi et al., 1995), Brachybacterium alimentarium CCM 4520T, Brachybacterium tyrofermentans CCM 4521T (Schubert et al., 1996), Brachybacterium fresconis DSM 14564T, Brachybacterium sacelli DSM 14566T (Heyrman et al., 2002) and Brachybacterium nesterenkovii CCM 2432, which had been reliably identified by DNA–DNA hybridizations (Takeuchi et al., 1995), were also studied.
Laboratory mice were killed with chloroform and the liver was prepared under semi-sterile conditions. Liver specimens were transferred to Brucella broth (Difco Laboratories) supplemented with 8 % fetal bovine serum (Life Technologies) and Skirrow selective supplement (Oxoid) and incubated under microaerobic conditions (90 % N2, 5 % CO2, 5 % H2 and residual O2) at 37 °C in an anaerobic jar (Oxoid) as reported by Fox et al. (1994). Samples of the enrichment culture were subcultured on sheep blood agar until pure cultures were obtained (Buczolits et al., 2001).
16S rDNA amplification and sequence comparisons were done as described previously (Buczolits et al., 2002). The 16S rDNA sequence of strain C3H-21T consisted of a fragment of 1429 bases (positions 7–1438, Escherichia coli numbering; Brosius et al., 1978). Highest but almost identical sequence similarities were found to B. sacelli LMG 20345T (97·8 %), B. nesterenkovii DSM 9573T (97·7 %), B. rhamnosum LMG 19848T (97·7 %), B. alimentarium CNRZ 925T (97·2 %) and B. fresconis LMG 20336T (97·2 %). Sequence similarities to other species of the genus Brachybacterium were in the narrow range of 96·7–96·9 %; sequence similarity to another species of the family Dermabacteraceae, Dermabacter hominis DSM 7083T, was 95·7 %. These results clearly demonstrated that strain C3H-21T is affiliated to the genus Brachybacterium and, since it exhibited almost identical sequence similarity values to three species of the genus, they suggested that it represents a novel species of the genus Brachybacterium. Phylogenetic analyses confirmed the view that strain C3H-21T is affiliated to the genus Brachybacterium (Fig. 1), but its position within the genus is not very clear since the branching order between many species of the genus was not supported by high bootstrap values (<70 %).
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), physiological and biochemical characterization have been described previously (Zlamala et al., 2002). Gram-staining, KOH test and aminopeptidase test were positive. No motility was observed by phase-contrast microscopy. Strain C3H-21T grew best on sheep blood agar and Brucella broth supplemented with 8 % fetal bovine serum (Buczolits et al., 2001) at 25–37 °C. Strain C3H-21T grew under aerobic conditions, but better growth was observed when it was incubated in an anaerobic jar under microaerobic conditions (90 % N2, 5 % CO2, 5 % H2 and residual O2). No growth occurred under anaerobic conditions. Other characteristics of strain C3H-21T and other representatives of the genus Brachybacterium are summarized in Table 1 and in the species description below. Based on its biochemical and physiological properties, strain C3H-21T is clearly distinguishable from the next related species.
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and the amino acids and peptides in peptidoglycan hydrolysates were analysed as described previously (Groth et al., 1997). The amino acids present in the peptidoglycan of strain C3H-21T were meso-diaminopimelic acid, alanine, glycine, aspartic acid and glutamic acid (molar ratio 1·2 : 1·6 : 1·2 : 1·0 : 2·0, respectively). On the basis of the molar ratios of the amino acids, the peptidoglycan type of the strain is A31.3 (DSMZ Catalogue of Strains, 7th edn, 2001). The peptidoglycan type of our isolate was variation A4 [meso-diaminopimelic acid-(D-Glu)2 type] (Schleifer & Kandler, 1972). The interpeptide bridge of strain C3H-21T contains D-asp-D-glu rather than D-glu-D-Glu. Strain C3H-21T shares this peptidoglycan type with B. alimentarium and B. tyrofermentans and it differentiates it from B. nesterenkovii, which lacks glycine and aspartic acid, and from B. faecium, B. fresconis, B. sacelli, B. rhamnosum, B. conglomeratum and Brachybacterium paraconglomeratum, which lack aspartic acid. Muramic acid residues of the peptidoglycan of strain C3H-21T are N-acetylated and not N-glycolated like other species of the genus Brachybacterium (Collins et al., 1988; Gvozdyak et al., 1992; Takeuchi et al., 1995; Schubert et al., 1996; Heyrman et al., 2002). These results indicate that strain C3H-21T is not affiliated to any established species of the genus Brachybacterium.
The quinone systems of strain C3H-21T and the other Brachybacterium strains were analysed according to Tindall (1990). Strain C3H-21T contained the major menaquinone MK-7 and minor amounts of menaquinone MK-8 and MK-6 (Table 1
). The quinone systems of strain C3H-21T and the other Brachybacterium strains were in excellent agreement with data from the literature (Collins et al., 1988; Gvozdyak et al., 1992; Takeuchi et al., 1995), but the quinone system of strain C3H-21T distinguishes it from B. alimentarium and B. sacelli, which were reported to have a quinone system with menaquinones MK-7 and MK-8 in a ratio of 2 : 1 (Schubert et al., 1996; Heyrman et al., 2002), and from B. fresconis, which is the Brachybacterium species that also, uniquely, contains minor amounts of menaquinone MK-7(H2) in its quinone system (Heyrman et al., 2002). Polar lipids were extracted and analysed by two-dimensional TLC according to Ventosa et al. (1993). Strain C3H-21T shared with other members of the genus Brachybacterium, which were also analysed, the genus-specific lipids diphosphatidylglycerol, phosphatidylglycerol and some unknown phospho- and glycolipids (Collins et al., 1988). The detection of additional lipids (Table 1) resulted in a unique polar lipid profile which appears to be useful for differentiating strain C3H-21T from other species of the genus Brachybacterium (Table 1). Cellular fatty acid methyl esters obtained from cells grown in Bacto tryptic soy broth at 28 °C by using the method of Stead et al. (1992) were analysed by GC (Groth et al., 1996). The predominant fatty acid in strain C3H-21T was anteiso-C15 : 0 (60·3 %). Additionally, considerable amounts of iso-C16 : 0 (7·2 %), iso-C14 : 0 (5·7 %), anteiso-C17 : 0 (5·3 %), C19 : 0 (5·3 %), iso-C15 : 0 (4·5 %), C18 : 1
7c (4·0 %) and an unknown acid (4·8 %) and minor amounts of C16 : 0 (1·0 %) and another unknown acid (1·9 %) were detected in strain C3H-21T. This fatty acid profile is in good agreement with the major characteristics of members of the genus Brachybacterium (Collins et al., 1988; Gvozdyak et al., 1992; Takeuchi et al., 1995; Schubert et al., 1996; Heyrman et al., 2002), although quantitative differences in the relative amounts of certain fatty acids may be useful for differentiation purposes. Mycolic acids were not detected, which were analysed according to Minnikin et al. (1980).
Extraction and detection of the polyamine patterns were performed as described previously (Busse & Auling, 1988; Altenburger et al., 1997). The polyamine pattern of strain C3H-21T consisted of major compounds spermine [7·0 µmol (g dry weight)-1] and spermidine [5·8 µmol (g dry weight)-1], and traces of putrescine and cadaverine [<0·03 µmol (g dry weight)-1]. To evaluate polyamine patterns for suitability in classification of Brachybacterium, the type species of the genus, B. faecium CCM 4372T, was analysed for its polyamine pattern as well. This strain also contained a polyamine pattern which was characterized by the major compounds spermidine [7·5 µmol (g dry weight)-1] and spermine [6·9 µmol (g dry weight)-1]. Additionally, minor amounts of putrescine [0·1 µmol (g dry weight)-1] and traces of cadaverine and diaminopropane were detected [<0·02 µmol (g dry weight)-1]. Among the class Actinobacteria, similar polyamine patterns have only been detected in species of certain genera of the family Microbacteriaceae, namely, Clavibacter, Rathayibacter and Curtobacterium (Altenburger et al., 1997), and genera of the family Propionibacteriaceae, namely, Propioniferax, Friedmanniella, Microlunatus, Luteococcus (Busse & Schumann, 1999) and Propionibacterium (Hamana, 1995), but these taxa can be easily distinguished from Brachybacterium based on their quinone systems and peptidoglycan composition. However, the overall polyamine contents in representatives of these taxa were reported to be significantly lower than those observed in strain C3H-21T and B. faecium CCM 4372T. These findings suggest that, in addition to the polyamine composition, the overall polyamine contents can be useful for discrimination of actinobacterial taxa and that species of the genus Brachybacterium contain a polyamine pattern which may be useful for their differentiation from other members of the class Actinobacteria, especially when analysed in combination with the quinone system and peptidoglycan composition.
Although strain C3H-21T had many of the characteristics of the genus Brachybacterium (Collins et al., 1988; Gvozdyak et al., 1992; Takeuchi et al., 1995; Schubert et al., 1996; Heyrman et al., 2002), its unique combination of chemotaxonomic characteristics indicated its separate position within the genus.
To confirm the distinct position of strain C3H-21T within the genus Brachybacterium, its protein pattern, which was obtained after SDS-PAGE (Stan-Lotter et al., 2002), was compared to reference strains, namely, B. sacelli DSM 14566T, B. nesterenkovii CCM 2432, B. rhamnosum DSM 10240T, B. alimentarium CCM 4520T and B. fresconis DSM 14564T. Cells were grown in PYES medium (g l-1: 0·3 % yeast extract, 0·3 % peptone from casein, 0·23 % Na2-succinat; pH 7·2), harvested by centrifugation (7000 g, 5 min), washed with 0·9 % (w/v) NaCl and suspended in fourfold-concentrated sample buffer (Laemmli, 1970) to a ratio of 200 mg wet weight (ml buffer)-1. Following four cycles of freezing–thawing, 3 volumes of water were added, and the samples were boiled for 5 min then centrifuged; supernatants were analysed by SDS-PAGE on 11 % polyacrylamide gels and Coomassie blue staining (Laemmli, 1970). Reproducibility of the protein extraction and electrophoretic procedures was confirmed by comparing duplicate extracts and by performing duplicate runs of a single extract on the same gel as well as on separate gels.
Electrophoretic protein patterns were recorded on an Umax Astra 1220 S scanner (Umax Systems) and analysed with the GELCOMPAR software package, Version 3.0 (Applied Maths). The software calculated the Pearson product moment correlation coefficient (r) between the samples and clustered the samples using the UPGMA. These examinations supported the separate position of strain C3H-21T within the genus Brachybacterium (Fig. 2).
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). Comparison of REP-PCR-generated fingerprints of strain C3H-21T, B. sacelli DSM 14566T, B. nesterenkovii CCM 2432, B. rhamnosum DSM 10240T, B. alimentarium CCM 4520T and B. fresconis DSM 14564T, which was done as described by Wieser & Busse (2000), revealed unique band patterns for each strain (Fig. I, available in IJSEM Online). Visual evaluation of the band patterns indicated that strain C3H-21T only shared with B. sacelli DSM 14566T a single band at approximately 400 bp.
Based on 16S rDNA sequence comparisons, strain C3H-21T occupies a separate position within the genus Brachybacterium. This is confirmed by its unique combination of chemotaxonomic characteristics (Table 1), protein pattern (Fig. 2), REP-PCR-generated genomic fingerprint (Fig. I, IJSEM Online) and physiological/biochemical traits (Table 1). In conclusion, we here describe a novel species of the genus Brachybacterium, for which we propose the name Brachybacterium muris.
Description of Brachybacterium muris sp. nov.
Brachybacterium muris (mu'ris. L. gen. n. muris of the mouse; the type strain was isolated from a mouse).
Cells are small coccoid to ovoid, 1·2–1·5 µm in diameter. Cells occur singly, in pairs or in agglomerates. Gram-positive and non-spore-forming. Motility is not observed. Cells grow best on sheep blood agar plates and Brucella broth supplemented with 8 % fetal bovine serum. Colonies on PYES agar are translucent, have light-yellow pigmentation and are circular, convex and smooth. Best growth is observed under microaerobic conditions, moderate growth is observed under aerobic conditions, but no growth occurs anaerobically. Colony diameters on sheep blood agar are 3–5 mm after 4 days incubation at 37 °C under microaerobic conditions. The temperature range for growth is 15–42 °C, with optimal growth between 25 and 37 °C; no growth at 4 °C. No growth is observed at pH 5·0. Can grow in the presence of up to 10 % NaCl. Catalase-positive. Oxidase-negative. Nitrate is reduced to nitrite. Physiological and biochemical traits are shown in Table 1. The diagnostic cell-wall diamino acid is meso-diaminopimelic acid and the peptidoglycan type is A31.3 (variation A4) containing the amino acids meso-diaminopimelic acid, alanine, glycine, aspartic acid and glutamic acid. Muramic acid residues are N-acetylated and not N-glycolated. The polar lipid profile is composed of diphosphatidylglycerol, phosphatidylglycerol, three unknown glycolipids, two unknown phospholipids and six unidentified polar lipids. Mycolic acids are absent. The fatty acid profile consists of the predominant compound anteiso-C15 : 0 with significant amounts of iso-C14 : 0, iso-C15 : 0, iso-C16 : 0, anteiso-C17 : 0 and C19 : 0. The principal menaquinone is MK-7; MK-8 and MK-6 are present in minor amounts. Spermine and spermidine are the predominant components of the polyamine pattern.
The type strain C3H-21T (=DSM 14560T=CCM 7047T) was isolated from the liver of a laboratory mouse strain.
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