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1 Laboratory of Bioresources, Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan
2 DADB, Service de Microbiologie, Hôpital Louis-Pasteur, Hôpitaux Civils, 68024 Colmar, France
3 Thailand Institute of Scientific and Technological Research (TISTR), 196 Phahonyothin Road, Chatuchak, Bangkok 10900, Thailand
Correspondence
Yi-Chueh Lin
yilin{at}genes.nig.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONNOTE ADDED IN PROOFREFERENCES |
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Published online ahead of print on 16 April 2004 as DOI 10.1099/ijs.0.02741-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences determined in this study are given in Fig. 2
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONNOTE ADDED IN PROOFREFERENCES |
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) and unsaturated major menaquinones (Collins & Jones, 1981). At first, the family Microbacteriaceae was proposed to accommodate the genera Agromyces, Aureobacterium, Clavibacter, Curtobacterium and Microbacterium (Park et al., 1993). On the basis of 16S rRNA gene sequence data, the family was found to accommodate the genera Agrococcus and Rathayibacter in addition to the above-mentioned genera (Stackebrandt et al., 1997). The genera Leucobacter (Takeuchi et al., 1996) and Cryobacterium (Suzuki et al., 1997) have also been shown to represent branches within the family Microbacteriaceae. It has been proposed that the genera Aureobacterium and Microbacterium should be united in the redefined genus Microbacterium on the basis of 16S rRNA gene sequence data and chemotaxonomic data (Takeuchi & Hatano, 1998). The new genera Frigoribacterium (Kämpfer et al., 2000) and Subtercola (Männistö et al., 2000) have been reported as psychrophilic members of the family. The genera Leifsonia (Evtushenko et al., 2000), Agreia (Evtushenko et al., 2001), Mycetocola (Tsukamoto et al., 2001), Okibacterium (Evtushenko et al., 2002) and Plantibacter (Behrendt et al., 2002) have also been shown to be members of the family Microbacteriaceae. The aim of the present study was to identify the seven isolates collected from various sources in the culture collection of the Institute of Applied Microbiology, University of Tokyo (Tokyo, Japan). Here we describe the physiological, chemotaxonomic and phylogenetic characteristics of these strains. On the basis of these data, six strains are proposed as constituting a novel genus, Zimmermannella gen. nov., containing four new species; the other strain is proposed to be a novel species, Leucobacter albus sp. nov.
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METHODS |
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. Strains IAM 14848T and IAM 14851T were isolated in our laboratory from soil from Thailand. The medium used for isolation was nutrient agar (Difco) containing 20 µg polymyxin B ml–1and 100 µg cycloheximide ml–1 and was incubated at 27 °C for 7 days. After colonies had formed, the Gram-positive strains were picked up. With the exception of strain IAM 14724T, the strains were grown in peptone/yeast extract broth supplemented with brain heart infusion (BHI) (Difco), i.e. 1 % peptone, 0·2 % yeast extract, 0·2 % NaCl, 0·2 % D-glucose, 0·2 % BHI, 1·5 % agar (pH 7·0) (PY–BHI medium) and nutrient agar medium containing 0·5 % peptone, 0·3 % meat extract, 0·3 % NaCl and 1·5 % agar (pH 7·0). Strain IAM 14724T was grown in PY–BHI medium to which 0·1 % MgSO4.7H2O had been added. All strains were cultured aerobically at 30 °C.
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Chemical analyses.
Cell walls were prepared from approximately 500 mg (dry weight) bacterial cells as described by Schleifer & Kandler (1972). Amino acids in an acid hydrolysate of the cell walls were identified by two-dimensional descending chromatography on cellulose TLC plates (Tokyo Kasei) by the method of Harper & Davis (1979) and by HPLC, as their phenylthiocarbamoyl derivatives, with a model LC-6AD HPLC apparatus (Shimadzu) equipped with a Wakopak WS-PTC column (Wako Pure Chemical Industries, 1989). Analysis of enantiomeric diamino acid isomers was performed according to Sasaki et al. (1998). Cell-wall sugars were analysed as described by Mikami & Ishida (1983). Fatty acids were extracted from dried cells, purified and then examined as described previously (Yokota et al., 1993). The glycolate test was performed by using the method of Uchida & Aida (1977).
G+C content and DNA–DNA relatedness.
Isolation and purification of chromosomal DNA and estimation of the DNA G+C content were performed by using the methods of Takagi et al. (1993). DNA relatedness values were determined as described by Ezaki et al. (1989).
16S rRNA gene sequence analyses.
The 16S rRNA gene was amplified by a PCR using prokaryotic 16S rRNA gene universal primers 8F (5'-AGAGTTTGATCCTGGCTCAG-3') and 1510R (5'-GGCTACCTTGTTACGA-3'). The PCR products were purified using a Sepharose Cl-2B gel (Pharmacia). Sequencing reactions were performed using the ABI PRISM BigDye Terminator cycle sequencing ready reaction kit (Applied Biosystems). The primers used for sequencing were 8F, 704R (5'-TCTACGCATTTCACC-3'), 520F (5'-CAGCAGCCGCCGTAATAC-3'), 1100R (5'-GGGTTGCGCTCGTTG-3'), 926F (5'-AAACTCAAAGGAATTGACGG-3') and 1510R. All PCRs were performed with a Perkin-Elmer Cetus model 9600 thermal cycler. Each extension product resulting from the sequencing reaction was purified through a Centri-Sep spin column (Applied Biosystems) and sequenced by using an ABI model 373S automated DNA sequencer.
Phylogenetic analysis.
The multiple alignment of sequences, calculation of nucleotide substitution rates (Knuc values; Kimura, 1980), construction of a neighbour-joining phylogenetic tree (Saitou & Nei, 1987) and bootstrap analysis with 1000 replicates for evolution of phylogenetic tree topology (Felsenstein, 1985) were carried out with the CLUSTAL W multiple sequence alignment program (Thompson et al., 1994). The NCBI and DDBJ accession numbers used in this analysis are given in Fig. 2. Arthrobacter globifomis ATCC 8010T (M23411) and Cellulomonas flavigena ATCC 482T (X79463) were used as the outgroup.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONNOTE ADDED IN PROOFREFERENCES |
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a). Cells of strains IAM 14726T, IAM 14724T, IAM 15030T and IAM 14851T were short rods, 0·3–0·4 µm wide and 0·5–1·1 µm long; cells of IAM 14848T, IAM 15028 and IAM 15029 were rods, 0·3–0·4 µm wide and 1·5–3 µm long in PY–BHI medium. Cells of strain IAM 14848T had a branched shape (Fig. 1b). The cells of all strains formed round, smooth, convex, white colonies. All strains were catalase-positive and negative for nitrate reduction (Table 2). Strains IAM 14848T, IAM 15028, IAM 15029 and IAM 14724T were positive for alkaline phosphatase activity. Strains IAM 14726T and IAM 14848T produced acid from rhamnose, and strain IAM 15028 produced acid from ribose. Strain IAM 15030T produced acid from D-glucose, D-fructose, D-mannose, rhamnose, inositol and mannitol. Strain IAM 14851T produced acid from glycerol, ribose and L-fucose.
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). Strains IAM 14726T and IAM 15030T had MK-9 as the major menaquinone, IAM 14724T had MK-10, while strains IAM 14848T, IAM 15028 and IAM 15029 had MK-8 and MK-9. In strain IAM 14851T, MK-11 was the major menaquinone. The cellular fatty acids of all of the strains mainly comprised anteiso-C15 : 0, C16 : 0, iso-C16 : 0 and anteiso-C17 : 0.
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). Most of the strains contained L-DAB, except for IAM 15030T and IAM 14726T. Strain IAM 15030T contained homoserine in addition to L-DAB. Strain IAM 14726T contained L-dab and D-DAB. The peptidoglycan of strain IAM 14726T contained glutamate, glycine, alanine and L-DAB in molar ratios of 1·0 : 1·0 : 0·8 : 1·8, corresponding to type B2
of Schleifer & Kandler (1972). Those of strains IAM 14724T, IAM 14848T, IAM 15028 and IAM 15029 contained these amino acids in nearly the same ratios. The peptidoglycan of strain IAM 15030T contained glutamate, glycine, alanine, L-DAB and homoserine in molar ratios of 1·0 : 1·9 : 0·8 : 0·9 : 0·2. The peptidoglycan of strain IAM 14851T contained glutamate, glycine, alanine, L-DAB and -aminobutyric acid in molar ratios of 1·0 : 1·1 : 1·8 : 0·8 : 0·7.
The cell-wall sugars of all the strains are shown in Table 3. The cell-wall sugars of strain IAM 14726T were rhamnose and 6-deoxytalose, while those of strain IAM 14724T were rhamnose, 6-deoxytalose and glucose. The cell-wall sugars of strains IAM 14848T, IAM 15028 and IAM 15029 were rhamnose and glucose, that of strain IAM 15030T was rhamnose, and those of strain IAM 14851T were rhamnose, galactose and glucose.
Phylogenetic analysis of the 16S rRNA gene
Nearly complete 16S rRNA gene nucleotide sequences (1480 bp) were determined for the seven strains. The phylogenetic tree constructed using the neighbour-joining method and Knuc values clearly shows that strain IAM 14851T is in the same cluster as Leucobacter komagatae IAM 1093T, with the other six strains occupying a distinct position in the family Microbacteriaceae with 100 % bootstrap confidence (Fig. 2).
The level of 16S rRNA gene sequence similarity between the isolates IAM 14851T and L. komagatae IAM 1093T was 98·2 %. Strains IAM 14726T and IAM 14724T showed 96·1–96·6 % 16S rRNA gene sequence similarity. The 16S rRNA genes of IAM 14848T, IAM 15028 and IAM 15029 showed 99·6–99·8 % similarity to each other and 96–98·1 % sequence similarity to the other three strains. The 16S rRNA gene of strain IAM 15030T showed 98 % sequence similarity to those of strains IAM 14848T, IAM 15028 and IAM 15029, and 96·3–96·6 % similarity to those of strains IAM 14726T and IAM 14724T.
G+C content and DNA–DNA relatedness
The DNA G+C contents were 66 mol% for strain IAM 14851T, 62 mol% for strains IAM 14848T, IAM 15028 and IAM 15029, 67 mol% for strains IAM 15030T and IAM 14726T and 68 mol% for strain IAM 14724T (Table 4). The levels of DNA relatedness were analysed, and the results are presented in Table 4. Three strains, IAM 14848T, IAM 15028 and IAM 15029, were found to have 75–82 % relatedness, while the other four strains showed little DNA relatedness. The DNA–DNA hybridization value between IAM 14851T and L. komagatae IAM 1093T was 40 % (Table 4).
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DISCUSSION |
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-aminobutyric acid is contained in the B-type peptidoglycan of the cell wall. The G+C content of the DNA of strain IAM 14851T (66 mol%) is also similar to that of L. komagatae. The 40 % level of DNA relatedness for IAM 14851T and L. komagatae IAM 1093T indicates that they belong to different species. According to Wayne et al. (1987), DNA–DNA relatedness of 70 % is considered to be the threshold value for the delineation of genomic species; thus, the 40 % level obtained is low enough to justify the separation of strain IAM 14851T and L. komagatae. The strain can also be differentiated from L. komagatae phenotypically (Table 2). Hence, strain IAM 14851T can be regarded as a novel Leucobacter species, for which we propose the name Leucobacter albus sp. nov.
The other six strains were collected from urine, wounds, soil, human blood and an unidentified species from the other culture collections. To clarify the taxonomic positions of these bacteria, their morphology, physiology and chemotaxonomic characteristics, together with DNA–DNA relatedness values and 16S rRNA gene sequence comparisons, were used in the present study. The strains were Gram-positive, aerobic, non-spore-forming, rod-shaped bacteria with a high G+C content (62–68 mol%). They also had the following characteristics: the major menaquinone was MK-8, -9 and/or -10, the diamino acid in the cell wall was DAB and the muramic acid in the peptidoglycan was of the acetyl type. The results of phylogenetic analysis of the 16S rRNA gene sequence revealed that these six strains form a monophyletic and distinct cluster, and that this cluster is independent from any of the subclusters corresponding to established genera within the family Microbacteriaceae. On the basis of the above data, these seven strains should belong to a novel genus in the family Microbacteriaceae. Hence, we propose a novel genus, Zimmermannella gen. nov. The characteristics used for differentiation at the genus level between the novel genus and other genera of the Microbacteriaceae are shown in Table 5. In the family Microbacteriaceae, most genera have DAB as a diamino acid and acetyl-type muramic acid in the peptidoglycan. However, the genus Zimmermannella can be distinguished from the other genera by the major menaquinone and the DNA G+C content. No genera of the Microbacteriaceae have shown MK-8 to MK-10 as the major menaquinones and G+C contents from 62 to 68 mol%, except the genus Zimmermannella.
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). These species can be distinguished from one another on the basis of both their morphological/biochemical characteristics and DNA–DNA relatedness values. We therefore propose the following classification: strains IAM 14726T and IAM 15030T are the type strains of Zimmermannella helvola sp. nov. and Zimmermannella faecalis sp. nov., respectively, strain IAM 14724T is the type strain of Zimmermannella alba sp. nov. and strains IAM 14848T, IAM 15028 and IAM 15029 are members of Zimmermannella bifida sp. nov. Differential characteristics for these four species are summarized in Table 3.
Description of Zimmermannella gen. nov.
Zimmermannella (Zim.mer.man'nel.la. N.L. fem. n. Zimmermannella named after O. E. R. Zimmermann, a German microbiologist, who first recognized the species ‘Brevibacterium helvolum’).
Cells are Gram-positive, aerobic, non-motile, short rods or rods. Endospores are not produced. Colonies are circular, convex, smooth and generally white on PY–BHI agar. The optimal temperature for growth is generally 30 °C. Catalase is always produced, while oxidase is only sometimes produced. Nitrate reduction, 
-galactosidase, 
-glucosidase and aesculin hydrolysis are not found. The cell-wall peptidoglycan contains DAB as a diamino acid, the major cell-wall sugar is rhamnose and the muramic acid of the cell wall is of the acetyl type. The major isoprenoid quinones are MK-8 to MK-10. The major fatty acids are C16 : 0, iso-C16 : 0, anteiso-C15 : 0 and anteiso-C17 : 0. The G+C content of the DNA is 62–68 mol%. Forms an independent phylogenetic cluster in the family Microbacteriaceae. The observed samples have been isolated from human wounds, urine, cow faeces, butter, human blood and soil. The type species is Zimmermannella helvola.
Description of Zimmermannella helvola sp. nov.
Zimmermannella helvola (hel'vo.la. L. fem. adj. helvola pale yellow).
Displays the following properties in addition to those given in the genus description. Cells are 0·3–0·5x0·8–1·1 µm and usually occur in pairs. Two rings are formed on one side of the cells. Oxidase is produced. Acid is produced from rhamnose. The following tests are negative: reduction of nitrite, nitrate respiration, liquefaction of gelatin, urease, alkaline phosphatase and acid production from glycerol, ribose, D-glucose, D-fructose, D-mannose, inositol, mannitol and D-fucose. The cell-wall peptidoglycan contains L- and D-DAB as diamino acids. The major isoprenoid quinone is MK-9. The G+C content of the DNA is 67 mol%.
The type strain, IAM 14726T (=NBRC 15775T=DSM 20419T=TISTR 1509T), was isolated from butter.
Description of Zimmermannella alba sp. nov.
Zimmermannella alba (al'ba. L. fem. adj. alba white).
Displays the following properties in addition to those given in the genus description. Cells are 0·3–0·4x0·5–1·1 µm. Oxidase is not produced. Alkaline phosphatase is found. The following tests are negative: reduction of nitrite, nitrate respiration, liquefaction of gelatin, urease and acid production from glycerol, ribose, D-glucose, D-fructose, D-mannose, rhamnose, inositol, mannitol and L-fucose. The cell-wall peptidoglycan contains L-DAB as a diamino acid The major isoprenoid quinone is MK-10. The G+C content of the DNA is 68 mol%.
The type strain, IAM 14724T (=NBRC 15616T=TISTR 1510T), was isolated from human urine.
Description of Zimmermannella bifida sp. nov.
Zimmermannella bifida (bi'fi.da. L. fem. adj. bifida divided into two parts).
Displays the following properties in addition to those given in the genus description. Cells are 0·3–0·4x1·5–3·0 µm. Branched shapes are formed. Oxidase is not produced. Alkaline phosphatase is produced. The following tests are negative for all strains: reduction of nitrite, nitrate respiration, liquefaction of gelatin, urease and acid production from glycerol, D-glucose, D-fructose, D-mannose, inositol, mannitol and L-fucose. The cell-wall peptidoglycan contains L-DAB as a diamino acid. The major isoprenoid quinones are MK-8 and MK-9. The G+C content of the DNA is 62 mol%.
The samples observed were isolated from human wounds, human blood and soil. The type strain is IAM 14848T (=TISTR 1511T).
Description of Zimmermannella faecalis sp. nov.
Zimmermannella faecalis (fae.ca'lis. N.L. fem. adj. faecalis faecal).
Displays the following properties in addition to those given in the genus description. Cells are 0·3–0·4x0·5–1·1 µm. Oxidase is produced. Acid is produced from D-glucose, D-fructose, D-mannose, rhamnose, inositol and mannitol. The following tests are negative: reduction of nitrite, nitrate respiration, liquefaction of gelatin, urease, alkaline phosphatase and acid production from glycerol, ribose and L-fucose. The cell-wall peptidoglycan contains L-DAB as a diamino acid. The major isoprenoid quinone is MK-9. The G+C content of the DNA is 67 mol%.
The type strain, IAM 15030T (=NBRC 15706T=ATCC 13722T=TISTR 1514T), was isolated from cow faeces.
Description of Leucobacter albus sp. nov.
Leucobacter albus (al'bus. L. masc. adj. albus white).
Cells are Gram-positive, aerobic rods, 0·3–0·4x0·5–1·1 µm, non-sporulating and non-motile. Smooth, white colonies are produced on PY–BHI agar. The optimal temperature for growth is 30 °C. Catalase is produced, but oxidase is not. Acid is produced from glycerol, ribose and L-fucose. The following tests are negative: reduction of nitrate or nitrite, nitrate respiration, liquefaction of gelatin, hydrolysis of aesculin, urease, alkaline phosphatase, -galactosidase and -glucosidase and acid production from D-glucose, D-fructose, D-mannose, rhamnose, inositol and mannitol. The cell-wall peptidoglycan contains L-DAB and -aminobutyric acid; the muramic acid of the cell wall is of the acetyl type. The major isoprenoid quinone is MK-11. The major fatty acids are anteiso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0. The G+C content of the DNA is 66 mol%.
The type strain, IAM 14851T (=TISTR 1515T), was isolated from soil.
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ACKNOWLEDGEMENTS |
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R. E. Muir and M.-W. Tan Leucobacter chromiireducens subsp. solipictus subsp. nov., a pigmented bacterium isolated from the nematode Caenorhabditis elegans, and emended description of L. chromiireducens Int J Syst Evol Microbiol, December 1, 2007; 57(12): 2770 - 2776. [Abstract] [Full Text] [PDF]
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Q. Zhang, C. Liu, Y. Tang, G. Zhou, P. Shen, C. Fang, and A. Yokota Hymenobacter xinjiangensis sp. nov., a radiation-resistant bacterium isolated from the desert of Xinjiang, China Int J Syst Evol Microbiol, August 1, 2007; 57(8): 1752 - 1756. [Abstract] [Full Text] [PDF]
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V. S. Somvanshi, E. Lang, P. Schumann, R. Pukall, R. M. Kroppenstedt, S. Ganguly, and E. Stackebrandt Leucobacter iarius sp. nov., in the family Microbacteriaceae Int J Syst Evol Microbiol, April 1, 2007; 57(4): 682 - 686. [Abstract] [Full Text] [PDF]
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N. Bora, M. Vancanneyt, R. Gelsomino, J. Swings, N. Brennan, T. M. Cogan, S. Larpin, N. Desmasures, F. E. Lechner, R. M. Kroppenstedt, et al. Agrococcus casei sp. nov., isolated from the surfaces of smear-ripened cheeses Int J Syst Evol Microbiol, January 1, 2007; 57(1): 92 - 97. [Abstract] [Full Text] [PDF]
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Y.-C. Lin and A. Yokota Plantibacter auratus sp. nov., in the family Microbacteriaceae. Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2337 - 2339. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, P. Schumann, and T.-K. Oh Yonghaparkia alkaliphila gen. nov., sp. nov., a novel member of the family Microbacteriaceae isolated from an alkaline soil. Int J Syst Evol Microbiol, October 1, 2006; 56(Pt 10): 2415 - 2420. [Abstract] [Full Text] [PDF]
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T. Ishikawa and A. Yokota Reclassification of Arthrobacter duodecadis Lochhead 1958 as Tetrasphaera duodecadis comb. nov. and emended description of the genus Tetrasphaera Int J Syst Evol Microbiol, June 1, 2006; 56(6): 1369 - 1373. [Abstract] [Full Text] [PDF]
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