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1 Department of Microbiology – Bioinformatics, Regeneration and Advanced Medical Science, Gifu University, Graduate School of Medicine, Tsukasa-machi 40, Gifu 500-8705, Japan
2 Department of Bacteriology, Osaka City University, Medical School, Abeno-ku, Osaka 545-8585, Japan
Correspondence
Takayuki Ezaki
tezaki{at}cc.gifu-u.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences of Arthrobacter russicus sp. nov. A1-3T, Rothia aeria sp. nov. A1-22T and Rhodococcus baikonurensis sp. nov. A1-17BT are AB071950–AB071952.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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reported that in-flight cross-contamination and build-up of pathogens were noted in the Apollo space station. The space station is a special environment with reduced gravity, and crews must live in a completely closed environment for extended periods of time. Because of the many unfavourable effects of space flight and mental stress, astronauts may suffer weakened immunocompetence and may even become infected by opportunistic pathogens (Criswell-Hudak, 1991). It is therefore essential to understand and control the microbial population in these environments. Bacteria were isolated from air and condensation water samples from the Russian space station Mir in 1997 and the bacterial population was analysed. Previous investigation had shown that bacteria from air samples were mainly Gram-positive, and most of the strains were opportunistic pathogens (Kawamura et al., 2001). A polyphasic taxonomic study showed that seven strains, belonging to six species, failed to match any established species. Three Gram-negative species of these isolates have been described elsewhere (Li et al., 2003, 2004). The taxonomic status of the four Gram-positive isolates was investigated in detail here.
Gram-positive bacteria have stronger resistance to dry conditions than do Gram-negative bacteria because of their firm cell-wall structure (Neidhardt, 1990). All four Gram-positive strains were isolated from air samples. These bacteria, drifting in the air of the space station, may become an infectious source and threaten the health of space-station astronauts, especially when astronauts have weakened immunocompetence. The four Gram-positive isolates were affiliated with the genera Rothia, Rhodococcus and Arthrobacter. As a result of polyphasic taxonomic study, these isolates should now be classified as the novel species Rothia aeria sp. nov., Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. After transfer to the laboratory, samples were cultured as described by Li et al. (2004) with incubation at 30 °C. Biochemical characterization of the isolates was performed using API CORYNE (API bioMérieux) and Biolog GP2 MicroPlate assay (Biolog). Oxidase activity was determined with oxidase test strips (Eiken Chemical). DNA was extracted as described by Ezaki et al. (1994).
Chemotaxonomic characterization.
Diamino acids were analysed by TLC as described by Kawamura et al. (1995). Other cell-wall amino acid analysis was performed as described by Komagata & Suzuki (1987). Briefly, bacteria were suspended in 10 ml 10 % trichloroacetic acid (w/v) and boiled for 30 min. The lysed bacteria were separated by centrifugation and the precipitate was then washed twice with distilled water and concentrated down at 10 000 r.p.m. for 10 min, resuspended in 10 ml PBS (0·145 M sodium chloride, 5 mM monobasic sodium phosphate, 8 mM dibasic sodium phosphate, pH 7·9) containing trypsin (2 mg ml–1) and incubated at 37 °C for 3 h. The precipitate was collected after centrifugation and washed twice with distilled water. It was then freeze-dried. Approximately 1 mg cell wall was hydrolysed for 18 h at 100 °C in 1 ml 6 M HCl. The hydrolysate was dried in a rotary evaporator and dissolved in 100 µl distilled water. Amino acids were mixed with 20 µl phenyl isothiocyanate solution (Wako) (ethanol/distilled water/trimethylamine/phenyl isothiocyanate, 7 : 1 : 1 : 1 by vol.) at room temperature for 20 min and analysed by HPLC (Hitachi UV detector L-7400) equipped with a Wakopak WS-PTC (4x200 mm) column.
Cellular fatty-acid compositions were measured using the Sherlock Microbial Identification system (MIDI) and method as described by Kosako et al. (2000). Mycolic acids were extracted and analysed as described by Nishiuchi et al. (1999). Polar lipids were identified as described by Minnikin et al. (1984). Isoprenoid quinone analysis was performed by reverse-phase TLC as described by Collins et al. (1977) and Yano et al. (1987).
Analysis of 16S rDNA sequence and DNA base composition.
The 16S rRNA gene was amplified with universal primers (forward: 5'-AGAGTTTGATCMTGGCTCAG-3'; reverse: 5'-ACGGGCGGTGTGTRC-3') and the PCR products for all isolates were sequenced in both directions. The sequences were analysed and trees generated as described by Li et al. (2004).
The G+C content was measured by HPLC as described by Ezaki et al. (1990). Escherichia coli was used as a standard (G+C content 51·19 mol%).
DNA–DNA hybridization.
Quantitative microplate DNA–DNA hybridization for selected strains was carried out as described by Ezaki et al. (1988, 1989). Hybridization experiments were carried out under optimal and stringent temperatures calculated from melting temperatures (Tm) based on the G+C content of each test strain.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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with Rothia dentocariosa as the type species. The phenotypic heterogeneity within the species has long been known (Lesher et al., 1974; Schofield & Schaal, 1981; Fotos et al., 1984), and the existence of a second genomovar was described by Kronvall et al. (1998). However, Rothia dentocariosa was recognized as the only species of the genus until Collins et al. (2000) described a novel species (Rothia nasimurium) and reclassified Stomatococcus mucilaginosus as Rothia mucilaginosa. Fan et al. (2002) proposed a further member, Rothia amarae.
Strain A1-17BT, isolated from air samples in the Russian space station Mir, formed a distinct phylogenetic subline and exhibited a specific association with genus Rothia (Fig. 1). 16S rDNA sequence similarity values between A1-17BT and its neighbours, Rothia dentocariosa genomovar II, Rothia dentocariosa, Rothia mucilaginosa, Rothia amarae and Rothia nasimurium, were respectively 99·8, 98·0, 96·4, 96·0 and 95·4 %, as determined by CLUSTAL W analysis. Similarity values to other members of the family Micrococcaceae were less than 95·0 %. Phylogenetic data showed that strain A1-17BT is a member of the genus Rothia. The G+C content is 57·8 mol%, which is within the range of 47–59 mol% observed in the genus (Bergan & Kocur, 1982; Gerencser & Bowden, 1986). This strain also showed morphological similarity to members of the genus Rothia (Georg & Brown, 1967) (see species description below).
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). HPLC analysis of the peptidoglycan showed that the amino acids glutamic acid, alanine and lysine occur in a molar ratio of 1 : 3 : 1; these results suggest that the interpeptide bridge contains alanine and that the peptidoglycan type is A3
-type (Schleifer & Kandler, 1972). The predominant isoprenoid quinone is menaquinone with seven isoprenoid units (MK-7), which is consistent with other related species in the genus Rothia (Table 1). Examination of the cellular fatty acids of A1-17BT revealed that the acids are predominantly of the iso- and anteiso-methyl-branching types. This is also similar to the composition of other species of Rothia (Table 1). The predominant polar lipids were phosphatidylglycerol and cardiolipin, with phosphatidylinositol as a minor component.
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-glucosidase and 
-glucosidase activities, hydrolysis of aesculin and acid production from glucose, maltose and sucrose; negative for -glucuronidase, -galactosidase, N-acetyl--glucosaminidase and urease activities and production of acid from ribose, xylose, mannitol, lactose and glycogen. These similar biochemical profiles support their relationship to these taxa. However, some common characteristics of strain A1-17BT and Rothia dentocariosa genomovar II differentiated them from Rothia dentocariosa and Rothia mucilaginosa (Table 1
). The results of the Biolog GP2 assay for strain A1-17BT are summarized in Table 2.
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), confirming that this strain represents a taxonomically independent species.
16S rDNA sequence similarity of 99·8 % and DNA–DNA relatedness of 100 % between strain A1-17BT and Rothia dentocariosa genomovar II indicated that they belong to the same species. Kronvall et al. (1998) suggested the possibility that Rothia dentocariosa genomovar II is a novel species of the genus. However, Rothia dentocariosa genomovar II has not been formally named as it could not be distinguished from authentic Rothia dentocariosa using API systems (Kronvall et al., 1998). In this study, strain A1-17BT, Rothia dentocariosa genomovar II and Rothia dentocariosa also showed the same biochemical characteristics using the API Coryne system, but the Biolog GP2 system clearly differentiated them biochemically from Rothia dentocariosa (Table 1). DNA hybridization data also supported strain A1-17BT and Rothia dentocariosa genomovar II as belonging to the same species and independent from other species of Rothia. Based on polyphasic taxonomic analysis, strain A1-17BT and Rothia dentocariosa genomovar II (strains CCUG 25688 and CCUG 33543) clearly merit classification as a novel species within the genus Rothia, Rothia aeria sp. nov.
Strain A1-22T
Sequence analysis by the FASTA search system on the DDBJ website showed that strain A1-22T was phylogenetically most closely related to the genus Rhodococcus. The phylogenetic position of strain A1-22T as analysed by CLUSTAL W software showed that it is closely related to Rhodococcus erythropolis, Rhodococcus globerulus, Rhodococcus marinonascens and Rhodococcus percolatus, with respective 16S rDNA sequence similarities of 99·2, 98·9, 97·6 and 97·0 % (Fig. 1). Similarity values to other Rhodococcus species and species of other genera were less than 97 % (data not shown). Phylogenetic analysis supported the affinity of strain A1-22T to genus Rhodococcus.
Strain A1-22T also showed similar phenotypic characteristics to Rhodococcus species (see species description below). Biochemically, strain A1-22T showed catalase and urease activities, but not oxidase activity, and was able to hydrolyse aesculin but not arbutin. The results of the Biolog GP2 analysis are shown in Table 2. Although strain A1-22T showed similar biochemical properties to its closest relative, Rhodococcus erythropolis, hydrolysis of arbutin and utilization of m-inositol enable them to be differentiated (Table 3).
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). HPLC analysis of the peptidoglycan showed that glycine, alanine and diaminopimelic acid are present in a 1 : 2 : 1 molar ratio. These results suggest that the peptidoglycan is A1
-type, which is consistent with Rhodococcus fascians (Goodfellow, 1984). The predominant isoprenoid quinone is MK-8(H2), which is consistent with the closely related species of the genus Rhodococcus (Goodfellow, 1986).
The cellular fatty acid composition of strain A1-22T was: 14 : 0, 5 %; cis-16 : 1, 9 %; 16 : 0, 41 %; cis-18 : 1, 18 %, 18 : 0, 4 %, tuberculostearic acid (10-methyl-18 : 0), 22 % (only components representing 
1 % of the total are reported). This composition is similar to that of some Rhodococcus species, but the strain can be differentiated from Rhodococcus erythropolis based on the content of 16 : 0 and 19 : 0 (22 and 10·9 % in Rhodococcus erythropolis; Yoon et al., 2000). The number of carbons in mycolic acids varies from 22 to 90, compared with the genera Corynebacterium (22–28), Gordonia (48–66), Mycobacterium (66–90), Nocardia (46–60) and Rhodococcus (32–66) (Goodfellow, 1986, 1992). The mycolic acid carbon chain of strain A1-22T determined by GLC/MS was 32–42 atoms in length with three double bonds, consistent with the genus Rhodococcus, with zero to four double bonds (Goodfellow, 1986). The cellular phospholipids were phosphatidylethanolamine, cardiolipin, phosphatidylinositol and phosphatidylinositol mannosides, again consistent with the properties of the genus Rhodococcus (Goodfellow, 1986).
DNA–DNA relatedness values of strain A1-22T with its closely related neighbours Rhodococcus erythropolis, Rhodococcus globerulus, Rhodococcus marinonascens and Rhodococcus percolatus were only 45·5, 35·3, 18·9 and 21·9 %. All hybridization rates were below the suggested threshold value (
70 %) (Grimont, 1999; Wayne et al., 1987), confirming that this strain represents a genetically independent species.
Based on polyphasic taxonomic results, strain A1-22T is affiliated with the genus Rhodococcus. However, based on its biochemical properties and chemotaxonomic characteristics, strain A1-22T is different from any established species of the genus. DNA–DNA hybridization data (<70 %) confirmed that strain A1-22T taxonomically represents an independent species. Thus, we propose the name Rhodococcus baikonurensis sp. nov. for this organism.
Strain A1-3T
Sequence analysis by the FASTA search system on the DDBJ website showed that strains A1-3T and A1-8 were phylogenetically most closely related to the genus Arthrobacter. A tree constructed using the neighbour-joining method depicting the phylogenetic position of strains A1-3T and A1-8 (Fig. 1) showed that strains A1-3T and A1-8 were closely related to Arthrobacter polychromogenes, Arthrobacter oxydans and Arthrobacter psychrolactophilus, with respective 16S sequence similarity of 96·6, 96·5 and 95·5 % (Table 4). 16S rDNA sequence similarity values to members of other genera were less than 95 %. Strains A1-3T and A1-8 exhibited an extremely high 16S rDNA sequence similarity of 99·9 %. These results clearly demonstrated that strains A1-3T and A1-8 belong to the genus Arthrobacter.
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). However, strains A1-3T and A1-8 can be differentiated biochemically from closely related species of the genus Arthrobacter (Table 4). The metabolic properties determined from the Biolog GP2 assay are shown in Table 2.
The cellular fatty acid content of strain A1-3T was as follows (only values 1 % reported): iso-15 : 0 (13-methyl-14 : 0), 1 %; anteiso-15 : 0 (12-methyl-14 : 0), 20 %; iso-16 : 0 (14-methyl-15 : 0), 4 %; 16 : 0, 2 %; iso-17 : 0 (15-methyl-16 : 0), 1 %; anteiso-17 : 0 (14-methyl-16 : 0), 64 %; anteiso-19 : 0 (16-methyl-18 : 0), 2 %; 2-OH 14 : 0, 1 %; and 2-OH 16 : 0, 4 %. This composition was consistent with that of members of the genus Arthrobacter, with anteiso-15 : 0 predominating. However, unlike many Arthrobacter species, including A. oxydans, Arthrobacter agilis and Arthrobacter roseus (Reddy et al., 2002; Kodama et al., 1992), strain A1-3T contained anteiso-19 : 0, 2-OH 14 : 0 and 2-OH 16 : 0. The predominant polar lipids were cardiolipin and phosphatidylinositol, with phosphatidylglycerol as a minor component. This composition is consistent with that of related species of the genus Arthrobacter (Reddy et al., 2002). Strains A1-3T and A1-8 lack diaminopimelic acid in their cell walls. The amino acids glutamic acid, alanine and lysine were detected in a molar ratio of 1 : 4 : 1 in the peptidoglycan. These results suggest that the interpeptide contains alanine and the peptidoglycan is A3-type (Kodama et al., 1992; Fiedler et al., 1973), consistent with the peptidoglycan type found in species of the A. polychromogenes group (Koch et al., 1995). The predominant isoprenoid quinone was MK-9(H2).
Strains A1-3T and A1-8 share DNA–DNA relatedness of 100 %, whereas these two strains showed only 9·8 % DNA–DNA relatedness with the nearest neighbour, A. polychromogenes. DNA–DNA hybridization is thought to be the superior method for the determination of relationships between bacteria (Stackebrandt & Goebel, 1994). These results demonstrate that strains A1-3T and A1-8 belong to the same genetic species, which is independent of the established species of the genus Arthrobacter.
Phenotypic and chemotaxonomic characteristics of strains A1-3T and A1-8 were also consistent with the description of the genus Arthrobacter and support the conclusion from the 16S rRNA alignment that these two strains belong to the genus Arthrobacter. However, biochemical characteristics and cellular fatty acid composition and DNA hybridization data sharply differentiate them from the closely related species A. polychromogenes. Therefore, the name Arthrobacter russicus sp. nov. is proposed for this species.
Description of Rothia aeria sp. nov.
Rothia aeria (aer'i.a. L. fem. adj. aeria of the air, referring to the isolation of the type strain from the air inside the Mir space station).
Grows well under aerobic conditions at 30 °C on BHI agar plates. Gram-positive cells appear coccoid, cocco-bacillary or filamentous. Young colonies are creamy white and smooth. Mature colonies are rough, dry, folded and convex and adhere to the agar medium such that they are not easily scraped off. Biochemical characteristics are summarized in Tables 1 and 2. Cell-wall peptidoglycan is A3-type. Predominant isoprenoid quinone is MK-7. Major cellular fatty acids are anteiso-15 : 0 (12-methyl-14 : 0), iso-16 : 0 (14-methyl-15 : 0) and anteiso-17 : 0 (14-methyl-18 : 0). Major polar lipids are phosphatidylglycerol and cardiolipin. The G+C content of the type strain is 57·8 mol%.
The type strain, A1-17BT (=GTC 867T=JCM 11412T=DSM 14556T), was isolated from an air sample from the Russian space station Mir. This species includes strains formerly categorized as Rothia dentocariosa genomovar II.
Description of Rhodococcus baikonurensis sp. nov.
Rhodococcus baikonurensis (bai.kon.ur.en'sis. N.L. masc. adj. baikonurensis of Baikonur, the town in Kazakhstan where the Mir space station was launched).
Grows well under aerobic conditions at 30 °C on BHI agar plates. A mixture of Gram-positive rods and cocci show elementary branching. Colonies are smooth, opaque and slightly pink. Biochemical characteristics are summarized in Tables 2 and 3. Diamino acid in the peptidoglycan is meso-diaminopimelic acid. Cell-wall peptidoglycan is A1-type. Predominant isoprenoid quinone is MK-8(H2). Major cellular fatty acids are 16 : 0, cis-18 : 1 and tuberculostearic acid (10-methyl-18 : 0). Mycolic acids contain 46–54 carbon atoms. Phospholipid composition is phosphatidylethanolamine, cardiolipin, phosphatidylinositol and phosphatidylinositol mannosides. The G+C content of the type strain is 55·5 mol%.
The type strain, A1-22T (=GTC 1041T=JCM 11411T=DSM 44587T), was isolated from an air sample from the Russian space station Mir.
Description of Arthrobacter russicus sp. nov.
Arthrobacter russicus [rus'sic.us. L. masc. adj. russicus pertaining to Russia (Russian space station)].
Grows well under aerobic conditions at 30 °C on BHI agar plates, but unable to grow at 37 °C. Gram-positive, non-motile, irregular rods, about 1·3–3·6 µm long and 0·5–0·9 µm wide. Circular, smooth and creamy colonies grow to a diameter of about 1·5 mm after 24 h. Biochemical characteristics are summarized in Tables 2 and 4. Cell-wall peptidoglycan is A3-type. Predominant isoprenoid quinone is MK-9(H2). Major cellular fatty acids are anteiso-15 : 0 (12-methyl-14 : 0) and anteiso-17 : 0 (14-methyl-16 : 0). Predominant polar lipids are cardiolipin and phosphatidylinositol. The G+C content of the type strain is 65·5 mol%.
The type strain, A1-3T (=GTC 863T=JCM 11414T=DSM 14555T), was isolated from an air sample from the Russian space station Mir.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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