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1 The Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan Institute of Microbiology, Yunnan University, Kunming, Yunnan, 650091, People's Republic of China
2 New Drug R & D, North China Pharmaceutic Corp., Shijiazhuang, 050015, People's Republic of China
Correspondence
Cheng-Lin Jiang
lihxu{at}ynu.edu.cn or
wjli{at}ynu.edu.cn
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ABSTRACT |
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7c (42·4 %) and C16 : 0 (28·1 %). The DNA G+C content was 62·4±0·3 mol%. Phylogenetic analysis based on the 16S rRNA gene sequence indicated that strain YIM 31775T should be placed within the family ‘Oxalobacteraceae’, in which it formed a distinct lineage. Based on the high 16S rRNA gene sequence divergence and phenotypic characteristics, it is proposed that strain YIM 31775T should be classified as representing a novel member of the family ‘Oxalobacteraceae’, for which the name Naxibacter alkalitolerans gen. nov., sp. nov. is proposed. The type strain is YIM 31775T (=CCTCC AA 204003T=KCTC 12194T).
The GenBank/EMBL/DDBJ accession number for the 16S RNA gene sequence of strain YIM 31775T is AY679161.
These authors contributed equally to this work. 
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MAIN TEXT |
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). 16S rRNA gene sequence analysis showed that the isolate belonged to the class ‘Betaproteobacteria’. The morphological, physiological and chemical characteristics, and phylogenetic analyses, showed that the strain should be classified as representing a novel member of the family ‘Oxalobacteraceae’, order ‘Burkholderiales’, class ‘Betaproteobacteria’ (Garrity & Holt, 2001). In this report we propose the name Naxibacter alkalitolerans gen. nov., sp. nov.
Strain YIM 31775T was isolated from a soil sample after incubation for 2 weeks at 28 °C on Water Proline agar (1 % proline/tap water). Biomass for molecular systematic and chemotaxonomic studies was obtained after incubation at 37 °C for 3 days in shake flasks containing tryptone soy broth (TSB; Oxoid). Colony morphology was determined after 3 days incubation at 28 °C on TSB agar. Colour determination was done with colour chips from the ISCC–NBS Colour Charts Standard Samples no. 2106 (Kelly, 1964). Gram (Lányí, 1987) and Ziehl-Neelsen (Gordon, 1967) preparations were observed by light microscopy (Olympus microscope BH-2). Cell motility was studied on Luria–Bertani swarming agar (0·3 %, w/v). Cellular morphology was studied by using a Hitachi H-800 transmission electron microscope.
The physiological and biochemical tests were all performed at 37 °C. Unless indicated otherwise, standard methods for phenotypic characterization of the strain were employed, as described by O'Brien & Colwell (1987). Catalase activity was determined by production of bubbles after the addition of a drop of 3 % H2O2. Some physiological properties were tested by using API ID32 E and API 20NE test kits (bioMérieux). The temperature range and the optimum temperature for growth were tested at 4–65 °C on TSB agar. The pH range and the optimum pH for growth were examined at pH 4·0–13·0, by using the following buffer system: pH 4·0–5·0: 0·1 M citric acid/0·1 M sodium citrate; pH 6·0–8·0: 0·1 M KH2PO4/0·1 M NaOH; pH 9·0–10·0: 0·1 M NaHCO3/0·1 M Na2CO3; pH 11·0: 0·05 M Na2HPO4/0·1 M NaOH; pH 12·0–13·0: 0·2 M KCl/0·2 M NaOH. Negative controls for each buffer were used and the final pH was determined by using an indicator of acidity (ORION). The liquid cultures were cultivated in tubes at 28 °C for 2–3 weeks. Tolerance to sodium chloride (1, 3, 7, 10 and 13 %) and phenol (0·1, 0·2, 0·5 and 1·0 %) was tested using TSB agar. Susceptibility to antibiotics was determined by using the disc-diffusion plate method. The following antibiotics were tested (concentration per millilitre in parentheses) with TSB agar: amikacin (30 µg), aureomycin (30 µg), ciprofloxacin (10 µg), chloramphenicol (30 µg), erythromycin (15 and 30 µg), gentamicin sulfate (10 µg), kanamycin (15 µg), netilmicin (10 µg), novobiocin (5 and 30 µg), oleandomycin (10 µg), penicillin G (10 U), polymyxin B (10 and 300 U), streptomycin sulfate (10 and 25 µg), terramycin (2·5 and 30 µg), tetracycline (10 and 30 µg), tobramycin sulfate (10 µg) and vancomycin (10 µg).
Biomass for quantitative fatty acid analysis was obtained from TSB agar that had been incubated for 3 days at 28 °C. Analysis of the whole-cell fatty acid pattern followed the MIDI system (Microbial ID) (Kroppenstedt, 1985; Meier et al., 1993). Polar lipids were determined by using the method of Minnikin et al. (1979). Isoprenoid quinones were isolated from lyophilized cells by using the method of Collins et al. (1977), and analysed by HPLC (Groth et al., 1997).
Bacterial genomic DNA preparation, PCR and 16S rRNA gene sequencing were carried out as described previously (Xu et al., 2003a; Cui et al., 2001). The nearly complete 16S rRNA gene sequence of strain YIM 31775T (1526 nucleotides) was aligned with corresponding almost complete sequences of members of the class ‘Betaproteobacteria’, retrieved from the DDBJ, EMBL and GenBank databases by using BLAST (Altschul et al., 1997) and BLAST 2 sequences (Tatusova & Madden, 1999). Following determination of the phylogenetic position within the class ‘Betaproteobacteria’, the dendrogram was restricted to the nearest neighbours. CLUSTAL W (Thompson et al., 1994) was used to estimate the evolutionary distances (Knuc value; Kimura, 1980) and similarity values were used to reconstruct a phylogenetic tree by the neighbour-joining method (Saitou & Nei, 1987). The topology of the tree was evaluated by performing a bootstrap analysis (Felsenstein, 1985) using 1000 resamplings. Ralstonia solanacearum ATCC 11696T (GenBank/EMBL/DDBJ accession no. X67036) was used as an outgroup. The chromosomal DNA for genomic DNA G+C content analysis was prepared by following the method of Marmur (1961). The DNA G+C content of strain YIM 31775T was determined by using the thermal denaturation method (Mandel & Marmur, 1968).
Colonies of strain YIM 31775T were 1·1–1·4 mm in diameter, circular, entire, convex, glistening, butyraceous and opaque, and had a pale white–yellow to straw-colour on nutrient agar plates. Cells were rod-shaped, 0·5–0·8x1·35–2·0 µm in size, Gram-negative, motile with one or more polar flagella, and chemo-organotrophic with respiratory-type metabolism. Spores and polyhydroxyalkanoates were not formed. The strain could not grow in the presence of sodium chloride at 3 %. The temperature range for growth was 4–55 °C, with optimum growth occurring at 28–37 °C. The pH range for growth was 6·5–12·0, with optimum growth occurring between pH 7·0 and 9·0. Tests for gelatin, melanin production and H2S production were positive; however, those for indole production, resistance to KCN, milk coagulation and peptonization were negative. Nitrate was not reduced to nitrite. Other physiological and biochemical results are listed in Table 1 and in the species description.
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). In the phylogenetic tree, strain YIM 31775T formed a distinct lineage within the family ‘Oxalobacteraceae’ (Garrity & Holt, 2001), and belonged to a cluster of species including Telluria mixta, Telluria chitinolytica, Massilia timonae, Duganella zoogloeoides, Janthinobacterium agaricidamnosum and Janthinobacterium lividum (see Fig. 1). The 16S rRNA gene sequence similarity values between strain YIM 31775T and its closest relatives, J. agaricidamnosum DSM 9628T, J. lividum DSM 1522T, D. zoogloeoides IAM 12670T and M. timonae CIP 105350T, were 95·5, 95·2, 95·0 and 94·9 %, respectively. The next closest relatives, Herbaspirillum, Telluria and Collimonas species, showed much lower similarity values (<93·6 %) (see Fig. 1). The 16S rRNA gene sequence similarity between strain YIM 31775T and the other ‘Betaproteobacteria’ reference strains was less than 91·6 %. The low level of sequence similarity between the novel strain and other bacteria belonging to the family ‘Oxalobacteraceae’ and related genera clearly demonstrates that YIM 31775T may be a representative of a new genus.
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7c, whereas those for the two type species of the genus Janthinobacterium (Lincoln et al., 1999) were C16 : 0, C16 : 17c and C17 : 0 cyclo. For the type strains of the genera Duganella (De Boer et al., 2004) and Massilia (Lindquist et al., 2003), the major fatty acid components were C16 : 0, C16 : 17c and C18 : 17c. Additionally, the presence of C18 : 19c in strain YIM 31775T was a characteristic that clearly distinguished the isolate from species of the genera Janthinobacterium, Duganella and Massilia (De Boer et al., 2004; Lincoln et al., 1999; Lindquist et al., 2003). The major hydroxyl fatty acids of the genus Duganella were C10 : 0 3-OH, C12 : 0 2-OH and C14 : 0 2-OH, whereas the novel isolate YIM 31775T had only C10 : 0 3-OH and C12 : 0 2-OH; this was an additional distinguishing characteristic.
The major isoprenoid quinone detected in strain YIM 31775T was Q-8 (93·4 %), and a minor amount of Q-7 (6·6 %) was also present. Polar lipids of strain YIM 31775T included phosphatidylglycerol, phosphatidylethanolamine and phosphatidylinositol mannosides. The predominant phosphatidylglycerol and phosphatidylethanolamine and the presence of ubiquinone 8 conform with the inclusion of strain YIM 31775T within the class ‘Betaproteobacteria’ (Wilkinson, 1988; Suzuki et al., 1993). The G+C content of genomic DNA of strain YIM 31775T was 62–63 mol%, which is similar to the G+C content of recognized species of the genera Janthinobacterium, Duganella and Massilia, but is notably lower than that of the genus Telluria (Table 1
).
From Table 1, it can also be seen that YIM 31775T shares some metabolic properties with strains of the genera Janthinobacterium, Duganella, Massilia and Telluria. However, the inability of strain YIM 31775T to metabolize rhamnose distinguishes it from the strains of these genera. The characteristics of starch hydrolysis, oxidase production and pigment production of strain YIM 31775T also differentiate it from the genera Janthinobacterium, Duganella, Massilia and Telluria (Table 1). Furthermore, unlike recognized species of the genera Janthinobacterium and Massilia, YIM 31775T is a soil bacterium with no apparent pathogenic or symbiotic relationship with mushrooms (Lincoln et al., 1999; La Scola et al., 1998). Therefore, the novel strain should not be classified within known genera of the family ‘Oxalobacteraceae’, order ‘Burkholderiales’, class ‘Betaproteobacteria’. On the basis of both the phylogenetic and phenotypic distinctions, we propose that strain YIM 31775T should be classified as representing a novel species within a new genus, for which the name Naxibacter alkalitolerans gen. nov., sp. nov. is proposed.
Description of Naxibacter gen. nov.
Naxibacter (Na.xi.bac'ter. N.L. n. Naxi referring to the Naxi nationality, who lived in Lijiang, Yunnan Province, China, from where the organism was isolated; n. bacter from Gr. n. baktron rod; N.L. masc. n. Naxibacter rod-shaped microbe from the place in which the Naxi nationality lived).
Gram-negative, oxidase-negative and catalase-positive. Aerobic and chemo-organotrophic. Cells are non-spore-forming rods with rounded ends, and motile with one or more polar flagella. The major cellular fatty acids are C16 : 17c and C16 : 0; the hydroxylated fatty acids are C10 : 0 3-OH and C12 : 0 2-OH. The main polar lipids are phosphatidylglycerol, phosphatidylethanolamine and phosphatidylinositol mannosides. Q-8 is the predominant respiratory quinone. The G+C content of genomic DNA is about 62–63 mol%. The genus is a member of the class ‘Betaproteobacteria’.
The type species is Naxibacter alkalitolerans.
Description of Naxibacter alkalitolerans sp. nov.
Naxibacter alkalitolerans (al.ka.li.to'le.rans. Arabic article al the; Arabic n. qaliy ashes of saltwort; French n. alcali alkali; N.L. n. alkali alkali; L. part. adj. tolerans tolerating; N.L. part. adj. alkalitolerans alkali-tolerating).
In addition to the characteristics that define the genus, the species has the characteristics described below. Colonies are 1·1–1·4 mm in diameter, circular, entire, convex, glistening, butyraceous, opaque and with pale white–yellow to straw-colour on nutrient agar plates. Cells are 0·45–0·8 µm wide and 1·35–2 µm long. Endospores are not observed. Polyhydroxyalkanoates are not formed. The isolate cannot grow in the presence of sodium chloride at 3 %. Temperature range for growth is 4–55 °C, with optimum growth occurring at 28–37 °C. pH range for growth is 6·5–12·0, with optimum growth occurring between pH 7·0 and 9·0. Dextrin, dulcitol, glycerol, inositol, mannose, mannitol, melibiose, melezitose, raffinose, ribose, salicin and xylitol are utilized as sole carbon and energy sources, but not adonitol, arabitol, galacturonate, inositol, oxalate, sorbitol or 5-ketogluconate. Nitrate, L-threonine, L-valine, L-hydroxyproline, L-lysine, L-tryptophan, L-proline, L-tyrosine, phenylalanine, L-histidine and L-asparagine (weak) are used as sole nitrogen sources, but not L-methionine, L-glutamic acid, glycine, L-arginine or L-cysteine. Urea, acetamide, xanthine, hypoxanthine, aesculin, keratin, chitin and DNA are hydrolysed. Tweens 20 and 80 are degraded, but not cellulose, starch, allantoin, glucosamine, amygdalin or adenine. Tests for gelatin, melanin production and H2S production are positive; however, those for nitrate reduction, indole production, resistance to KCN, milk coagulation and peptonization are negative. Tests for lipase, ornithine decarboxylase, 
-glucosidase, -galactosidase, 
-glucosidase and -galactosidase are positive. Tests for arginine dihydrolase, lysine decarboxylase and N-acetyl--glucosaminidase are negative. Resistant to lysozyme, penicillin G, vancomycin, polymyxin B, tobramycin sulfate, gentamicin sulfate, netilmicin, oleandomycin and ciprofloxacin (weak), but sensitive to erythromycin, terramycin, aureomycin, tetracycline, streptomycin sulfate, amikacin, novobiocin, kanamycin, nalidixic acid and chloramphenicol. The cellular fatty acid profiles are C16 : 17c (42·4 %), C16 : 0 (28·1 %), C17 : 0 cyclo (6·8 %), C12 : 0 (6·1 %), C18 : 17c (4·3 %), C10 : 0 3-OH (4·2 %), C14 : 0 (3·4 %), C18 : 19c (1·2 %), C10 : 0 (0·5 %), C18 : 0 (0·4 %), C12 : 0 2-OH (0·3 %) and C15 : 0 (0·2 %). The isoprenoid quinones are Q-8 (93·4 %) and Q-7 (6·6 %). The phospholipids are phosphatidylglycerol, phosphatidylethanolamine and phosphatidylinositol mannosides. The G+C content of genomic DNA is 62·4±0·3 mol%.
The type strain is YIM 31775T (=CCTCC AA 204003T=KCTC 12194T), which was isolated from soil in Lijiang, Yunnan Province, China.
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ACKNOWLEDGEMENTS |
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R. Liu, H. Liu, H. Feng, X. Wang, C.-X. Zhang, K.-Y. Zhang, and R. Lai Pseudomonas duriflava sp. nov., isolated from a desert soil Int J Syst Evol Microbiol, June 1, 2008; 58(6): 1404 - 1408. [Abstract] [Full Text] [PDF]
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R. Liu, H. Liu, C.-X. Zhang, S.-Y. Yang, X.-H. Liu, K.-Y. Zhang, and R. Lai Sphingobacterium siyangense sp. nov., isolated from farm soil Int J Syst Evol Microbiol, June 1, 2008; 58(6): 1458 - 1462. [Abstract] [Full Text] [PDF]
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W.-J. Li, P. Xu, P. Schumann, Y.-Q. Zhang, R. Pukall, L.-H. Xu, E. Stackebrandt, and C.-L. Jiang Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia Int J Syst Evol Microbiol, July 1, 2007; 57(7): 1424 - 1428. [Abstract] [Full Text] [PDF]
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P. Kampfer, R. Rossello-Mora, M. Hermansson, F. Persson, B. Huber, E. Falsen, and H.-J. Busse Undibacterium pigrum gen. nov., sp. nov., isolated from drinking water Int J Syst Evol Microbiol, July 1, 2007; 57(7): 1510 - 1515. [Abstract] [Full Text] [PDF]
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Y.-Q. Zhang, C.-H. Sun, W.-J. Li, L.-Y. Yu, J.-Q. Zhou, Y.-Q. Zhang, L.-H. Xu, and C.-L. Jiang Deinococcus yunweiensis sp. nov., a gamma- and UV-radiation-resistant bacterium from China Int J Syst Evol Microbiol, February 1, 2007; 57(2): 370 - 375. [Abstract] [Full Text] [PDF]
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W.-J. Li, Y.-Q. Zhang, P. Schumann, X.-P. Tian, Y.-Q. Zhang, L.-H. Xu, and C.-L. Jiang Sinococcus qinghaiensis gen. nov., sp. nov., a novel member of the order Bacillales from a saline soil in China Int J Syst Evol Microbiol, June 1, 2006; 56(6): 1189 - 1192. [Abstract] [Full Text] [PDF]
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W.-J. Li, Y.-Q. Zhang, P. Schumann, H.-H. Chen, W. N. Hozzein, X.-P. Tian, L.-H. Xu, and C.-L. Jiang Kocuria aegyptia sp. nov., a novel actinobacterium isolated from a saline, alkaline desert soil in Egypt. Int J Syst Evol Microbiol, April 1, 2006; 56(Pt 4): 733 - 737. [Abstract] [Full Text] [PDF]
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Y.-Q. Zhang, W.-J. Li, K.-Y. Zhang, X.-P. Tian, Y. Jiang, L.-H. Xu, C.-L. Jiang, and R. Lai Massilia dura sp. nov., Massilia albidiflava sp. nov., Massilia plicata sp. nov. and Massilia lutea sp. nov., isolated from soils in China Int J Syst Evol Microbiol, February 1, 2006; 56(2): 459 - 463. [Abstract] [Full Text] [PDF]
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