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1 Department of Soil Environmental Science, College of Agriculture and Natural Resources, National Chung Hsing University, Taichung, Taiwan
2 Laboratory of Microbiology, Department of Seafood Science, National Kaohsiung Marine University, Kaohsiung City 811, Taiwan
3 Department of Marine Biotechnology, National Kaohsiung Marine University, Kaohsiung, Taiwan
4 Graduate School of Biotechnology and Bioinformatics, Yuan-Ze University, Chung-Li, Taoyuan 320, Taiwan
Correspondence
Wen-Ming Chen
p62365{at}ms28.hinet.net
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with meso-diaminopimelic acid as the diagnostic cell-wall diamino acid. The isolate contained MK-7 as the major component of the quinone system. The polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, and unidentified phospholipids and glycolipids. The predominant fatty acid was anteiso-C15 : 0 (59.5 %); significant amounts of iso-C16 : 0 (9.4 %), iso-C14 : 0 (9.5 %) and anteiso-C17 : 0 (10.8 %) were also present. The isolate was also distinguished from recognized members of the genus Brachybacterium on the basis of several phenotypic and biochemical characteristics. It is evident from the genotypic, chemotaxonomic and phenotypic data that isolate phenol-AT represents a novel species of the genus Brachybacterium, for which the name Brachybacterium phenoliresistens sp. nov. is proposed. The type strain is phenol-AT (=LMG 23707T=BCRC 17589T).
A figure showing the polar lipid profile of strain phenol-AT and a table detailing the fatty-acid profile of strain phenol-AT in comparison with recognized members of the genus Brachybacterium are available as supplementary material with the online version of this paper.
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, belongs to the family Dermabacteraceae, class Actinobacteria. At the time of writing, the genus Brachybacterium encompasses ten recognized species: Brachybacterium alimentarium, B. conglomeratum, B. faecium, B. fresconis, B. muris, B. nesterenkovii, B. paraconglomeratum, B. rhamnosum, B. sacelli and B. tyrofermentans. The aim of the present study was to determine the taxonomic position of strain phenol-AT, which was isolated from an oil-contaminated coastal sand sample. A phenol-resistant bacterial strain, designated phenol-AT, was isolated on nutrient agar (BD Difco) supplemented with 3 % (w/v) NaCl and 0.05 % (w/v) phenol from a contaminated coastal sand sample collected from Pingtung County, Taiwan. The organism was maintained and subcultivated further on marine agar 2216 (BD Difco) or in marine broth 2216 (BD Difco). The novel strain was preserved at –80 °C in a 20 % (v/v) glycerol suspension in marine broth 2216 or by lyophilization.
The bacterial cells were observed via phase-contrast microscopy (DM 2000; Leica) in the lag, exponential and stationary phases of growth to ascertain their morphology. Motility of cells was tested by use of a hanging-drop method. Flagellum staining was performed by using Spot Test Flagella Stain (BD Difco). The Gram Stain Set (BD Difco) and Ryu non-staining KOH method (Powers, 1995) were used to ascertain the Gram reaction. Accumulation of poly-
-hydroxybutyrate granules was tested via light microscopy after staining cells with Sudan black. Colony morphology was studied by using a stereoscopic microscope (SMZ 800; Nikon). The presence of flexirubin-type pigments was investigated as described by Reichenbach (1992) and Bernardet et al. (2002). The pH range for growth was examined in marine broth 2216 medium by using appropriate biological buffers (pH 4–10 at intervals of 1.0 pH units) (Chung et al., 1995). Tolerance to various levels of NaCl was tested in nutrient broth prepared according to the formula of the Difco medium, but the NaCl concentrations were altered as required (0, 0.5 and 1.0–10 %, w/v, at intervals of 1.0 %). Growth at various temperatures (4–45 °C) was measured on marine broth 2216. Growth was examined by measuring the turbidity (OD600) of cultures grown over various pH, NaCl and temperature ranges. Anaerobic cultivation was performed on marine agar 2216 by using an Oxoid AnaeroGen system.
Extraction of genomic DNA, PCR amplification and sequencing of the 16S rRNA gene were carried out as described by Chen et al. (2001). The 16S rRNA gene sequence of strain phenol-AT was obtained by using a DNA sequencer (ABI PRISM 310; Applied Biosystems) and the sequence was then assembled by using the Fragment Assembly System program in the Wisconsin Package 9.1 (GCG, 1995). A nearly complete 16S rRNA gene sequence (1457 nt) of strain phenol-AT was compared with 16S rRNA gene sequences available from the RDP, GenBank and EzTaxon (Chun et al., 2007) databases. Multiple sequence alignments including strain phenol-AT and its closest relatives were performed by using BioEdit software (Hall, 1999) and MEGA version 3.1 (Kumar et al., 2004). Phylogenetic trees were inferred by using the maximum-likelihood (Felsenstein, 1981), maximum-parsimony (Fitch, 1971) and neighbour-joining (Saitou & Nei, 1987) algorithms. An evolutionary distance matrix was generated for the neighbour-joining algorithm according to the Jukes & Cantor (1969) distance model, and bootstrap analysis for the neighbour-joining tree was performed based on 1000 resamplings. A comparison of the 16S rRNA gene sequence of strain phenol-AT with those of members of the genera classified in the family Dermabacteraceae, class Actinobacteria, showed that the novel strain fell within the evolutionary radiation occupied by the genus Brachybacterium (Fig. 1). In the phylogenetic tree based on the neighbour-joining algorithm, strain phenol-AT formed a coherent cluster with B. nesterenkovii DSM 9573T, B. rhamnosum LMG 19848T and B. muris C3H-21T, but its position within the genus was not particularly clear as the branching order between many species of the genus was not supported by bootstrap values above 50 %. Similar tree topologies were obtained in phylogenetic trees generated with the maximum-parsimony and maximum-likelihood algorithms (data not shown). Based on 16S rRNA gene sequence similarity calculations, strain phenol-AT was most closely related to B. sacelli LMG 20345T (97.6 %), B. nesterenkovii DSM 9573T (97.0 %), B. rhamnosum LMG 19848T (96.9 %), B. paraconglomeratum LMG 19861T (96.8 %), B. fresconis LMG 20336T (96.3 %), B. faecium DSM 4810T (96.5 %), B. alimentarium CNRZ 925T (96.4 %), B. conglomeratum NCIB 9859 (96.4 %), B. muris C3H-21T (96.3 %) and B. tyrofermentans CNRZ 926T (96.3 %). The level of gene sequence similarity between strain phenol-AT and Dermabacter hominis DSM 7083T, a species from another genus within the family Dermabacteraceae, was only 95.1 %.
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. The level of hybridization was calculated by means of triplicate experiments. The separate species status of strain phenol-AT was demonstrated by the hybridization values obtained when it was hybridized with B. rhamnosum DSM 10240T, B. nesterenkovii DSM 9573T and B. muris DSM 15460T, which showed only 20.6±3.1, 15.0±3.6 and 11.2±2.7 % DNA–DNA relatedness to strain phenol-AT, respectively. These DNA–DNA relatedness values were significantly lower than that accepted as demarcating species (Wayne et al., 1987). Although strain phenol-AT showed highest 16S rRNA gene sequence similarity to B. sacelli LMG 20345T (97.6 %), DNA–DNA hybridization was not carried out because strain phenol-AT formed a separate subclade in the phylogenetic tree with a bootstrap value <50 % (Fig. 1
). Based on the above DNA–DNA relatedness data, strain phenol-AT warrants description as representing a novel species in the genus Brachybacterium.
The DNA G+C content of strain phenol-AT was estimated from duplicate experiments as described by Mesbah et al. (1989). The nucleoside mixture was separated with an HPLC system. The DNA G+C content of strain phenol-AT was 70.8 (±0.5) mol%, consistent with previously reported values for members of the genus Brachybacterium (68.6–73 mol%; Table 1).
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). Polar lipids were extracted and analysed by two-dimensional TLC according to Embley & Wait (1994). Purified cell-wall preparations were obtained by the method of Schleifer & Kandler (1972) and the amino acids in peptidoglycan hydrolysates were analysed as described by Schleifer (1985). Menaquinones were extracted and analysed by HPLC as described by Collins (1994) along with those from B. muris DSM 15460T, B. nesterenkovii DSM 9573T and B. rhamnosum DSM 10240T as reference strains. The predominant fatty acids in strain phenol-AT were anteiso-C15 : 0 (59.5 %), anteiso-C17 : 0 (10.8 %), iso-C14 : 0 (9.5 %) and iso-C16 : 0 (9.4 %) (see Supplementary Table S1 in IJSEM Online). 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; Buczolits et al., 2003). Strain phenol-AT contained MK-7 as the major component of the quinone system, as found for other species of the genus Brachybacterium (Takeuchi et al., 1995; Buczolits et al., 2003). Diphosphatidylglycerol and phosphatidylglycerol were the predominant polar lipids. In addition, four unknown glycolipids and one unknown phospholipid were detected. These data are again similar to those for other members of the genus Brachybacterium (Collins et al., 1988; Takeuchi et al., 1995; Buczolits et al., 2003) (see Supplementary Fig. S1 in IJSEM Online). The characteristic cell-wall amino acids for strain phenol-AT were meso-diaminopimelic acid, alanine, glycine, aspartic acid and glutamic acid. The peptidoglycan type was variant A4 (Schleifer & Kandler, 1972), consistent with other members of the genus Brachybacterium (Gvozdyak et al., 1992; Schubert et al., 1996; Heyrman et al., 2002; Buczolits et al., 2003). However, phenol-AT could be differentiated from B. nesterenkovii based on the presence of glycine and aspartic acid, and from B. conglomeratum, B. faecium, B. fresconis, B. paraconglomeratum, B. rhamnosum and B. sacelli based on the presence of aspartic acid (Table 1).
Strain phenol-AT was examined for a broad range of phenotypic properties. Catalase, oxidase, DNase and lipase activity, motility, production of acid from various carbohydrates, and hydrolysis of starch, casein and Tweens 20, 40, 60 and 80 were determined according to standard methods (Gerhardt et al., 1994; Lanyi, 1987; MacFaddin, 2000). Additional biochemical tests were performed by using the API Coryne, API 20E, API ZYM (all bioMérieux) and Biolog GP2 (Biolog) microtest systems according to the methods outlined by the manufacturers. Sensitivity to antibiotics was examined after spreading cells (0.5 McFarland units) on marine 2216 agar plates. The antibiotic discs contained the following: ampicillin (10 µg), chloramphenicol (30 µg), erythromycin (15 µg), gentamicin (10 µg), kanamycin (30 µg), nalidixic acid (30 µg), novobiocin (30 µg), rifampicin (5 µg), penicillin G (10 U), streptomycin (10 µg) or tetracycline (30 µg). The effect of antibiotics on cell growth was assessed after 3 days incubation and susceptibility was scored based on the distance from the edge of any clear zone to that of the disc. If the distance was greater than 3 mm, the strain was classified as susceptible, 1–3 mm, it was classified as moderately susceptible and if the clear zone was less than 1 mm, it was considered resistant. Detailed results of the biochemical characterization of strain phenol-AT are provided in Table 1 and in the species description below. A comparison of the phenotypic characteristics of strain phenol-AT with those of the type strains of related Brachybacterium species is presented in Table 1.
Based on 16S rRNA gene sequence comparisons, strain phenol-AT occupies a separate position within the genus Brachybacterium. This is confirmed by its unique combination of chemotaxonomic characteristics (Table 1 and Supplementary Table S1) and biochemical traits (Table 1). It is clear from the genotypic and phenotypic data presented that strain phenol-AT represents a novel species in the genus Brachybacterium, for which the name Brachybacterium phenoliresistens sp. nov. is proposed.
Description of Brachybacterium phenoliresistens sp. nov.
Brachybacterium phenoliresistens (phe.nol.i.res.ist.ens. N.L. neut. n. phenol phenol; L. part. adj. resistens resisting; N.L. part. adj. phenoliresistens phenol resisting, referring to the organism's ability to resist phenol).
Cells are small, coccoid to ovoid shaped, 0.8–1.3 µm in diameter. Cells occur singly, in pairs or as agglomerates. Facultatively anaerobic, Gram-positive (Gram staining and KOH test), non-motile and non-spore-forming. Colonies on marine 2216 agar are pale yellow, circular and convex in shape with entire edges. Colonies are approximately 0.9–2.1 mm in diameter on marine 2216 agar after 48 h incubation at 28 °C. No accumulation of poly--hydroxybutyrate granules is observed. Flexirubin-type pigments are present. Optimum growth occurs aerobically, while only moderate anaerobic growth is observed. Good growth occurs at temperatures of 4–40 °C, 0.5–7.0 % NaCl and pH 5–10. Optimum growth occurs at 28–35 °C, 2–3 % NaCl and pH 7.0. Acid is produced from arabinose, fructose, mannose, raffinose, rhamnose, sucrose, xylose, cellobiose, galactose, glucose, lactose and trehalose, but not from ribose or sorbitol. Positive for catalase, DNase, and hydrolysis of starch and Tween 20. Weakly positive for hydrolysis of casein and Tween 40. Negative for oxidase, nitrate reduction, nitrite reduction, lipase (corn oil) and hydrolysis of Tweens 60 and 80. In the API Coryne system, positive for hydrolysis of pyrazinamidase, pyrrolidonyl arylamidase, alkaline phosphatase, -glucuronidase, -galactosidase, 
-glucosidase, N-acetyl--glucosaminidase and aesculin and acid production from D-glucose, D-xylose, D-mannitol, maltose, D-lactose and sucrose. Negative for nitrate reduction, urease, gelatin hydrolysis and acid production from D-ribose and glycogen. With the API 20E system, positive for ONPG test, acetoin production and acid production from glucose, mannitol, inositol, rhamnose, sucrose, amygdalin and arabinose, but negative for nitrate reduction, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, citrate utilization, H2S production, urease, tryptophan deaminase, indole production, gelatinase and acid production from sorbitol and melibiose. Positive enzyme reactions (API ZYM) for alkaline phosphatase, C4 esterase, C8 lipase, leucine arylamidase, -galactosidase, -galactosidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase, weak positive reactions for C14 lipase, valine arylamidase, cystine arylamidase, acid phosphatase, naphthol-AS-BI-phosphohydrolase and -glucuronidase, but negative reactions for trypsin and -chymotrypsin. The following carbon substrates (Biolog GP2) are oxidized: -cyclodextrin, dextrin, glycogen, Tween 40, N-acetyl-D-glucosamine, L-arabinose, D-arabitol, arbutin, D-cellobiose, D-fructose, D-galactose, gentiobiose, -D-glucose, maltose, maltotriose, D-mannitol, D-mannose, D-melezitose, methyl -D-glucoside, palatinose, D-psicose, D-raffinose, salicin, D-sorbitol, stachyose, sucrose, trehalose, turanose, xylitol, pyruvic acid methyl ester, glycerol, adenosine and 2'-deoxyadenosine. Unable to oxidize -cyclodextrin, inulin, mannan, Tween 80, N-acetyl--D-mannosamine, amygdalin, L-fucose, D-galacturonic acid, D-gluconic acid, myo-inositol, -D-lactose, lactulose, D-melibiose, methyl -D-galactoside, methyl -D-galactoside, 3-methyl D-glucose, methyl -D-glucoside, methyl -D-mannoside, L-rhamnose, D-ribose, sedoheptulosan, D-tagatose, D-xylose, acetic acid, -hydroxybutyric acid, -hydroxybutyric acid, -hydroxybutyric acid, p-hydroxyphenylacetic acid, -ketoglutaric acid, -ketovaleric acid, lactamide, D-lactic acid methyl ester, L-lactic acid, D-malic acid, L-malic acid, succinic acid monomethyl ester, propionic acid, pyruvic acid, succinamic acid, succinic acid, N-acetyl-L-glutamic acid, L-alaninamide, D-alanine, L-alanine, L-alanyl glycine, L-asparagine, L-glutamic acid, glycyl L-glutamic acid, L-pyroglutamic acid, L-serine, putrescine, 2,3-butanediol, inosine, thymidine, uridine, adenosine, uridine 5'-monophosphate, D-fructose 6-phosphate, -D-glucose 1-phosphate, D-glucose 6-phosphate or DL--glycerol phosphate. Resistant to ampicillin, gentamicin, nalidixic acid and tetracycline, but sensitive to chloramphenicol, erythromycin, kanamycin, novobiocin, penicillin G, rifampicin and streptomycin. The diagnostic cell-wall diamino acid is meso-diaminopimelic acid and the peptidoglycan type is variation A4 containing amino acids meso-diaminopimelic acid, alanine, glycine, aspartic acid and glutamic acid. The polar lipid profile consists of diphosphatidylglycerol, phosphatidylglycerol, three unknown glycolipids and one unknown phospholipid. The predominant fatty acid is anteiso-C15 : 0 with significant amounts of iso-C16 : 0, iso-C14 : 0 and anteiso-C17 : 0. The major menaquinone is MK-7. DNA G+C content is 70.8 mol%.
The type strain, phenol-AT (=LMG 23707T=BCRC 17589T), was isolated from oil-contaminated coastal sand, Pingtung County, Taiwan.
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ACKNOWLEDGEMENTS |
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