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Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
Correspondence
Jung-Hoon Yoon
jhyoon{at}kribb.re.kr
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7c and 11-methyl C18 : 17c as the major fatty acids. The major polar lipids were phosphatidylcholine, phosphatidylglycerol, phosphatidylethanolamine, two unidentified lipids and an aminolipid. The DNA G+C content was 64.9 mol%. A neighbour-joining phylogenetic tree based on 16S rRNA gene sequences showed that strain TF-218T is phylogenetically closely related to the genera Phaeobacter, Leisingera and Marinovum of the Alphaproteobacteria. The phylogenetic and chemotaxonomic similarities suggest that strain TF-218T represents a member of the genus Phaeobacter. DNA–DNA relatedness data and differential phenotypic properties, together with the phylogenetic distinctiveness, demonstrated that strain TF-218T differs from the recognized Phaeobacter species. On the basis of the phenotypic, chemotaxonomic and phylogenetic data, strain TF-218T represents a novel species of the genus Phaeobacter, for which the name Phaeobacter daeponensis sp. nov. is proposed. The type strain is TF-218T (=KCTC 12794T=JCM 13606T).
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with descriptions of two species, Roseobacter litoralis and Roseobacter denitrificans. Subsequently, two other Roseobacter species, Roseobacter algicola (Lafay et al., 1995) and Roseobacter gallaeciensis (Ruiz-Ponte et al., 1998), were described. Roseobacter algicola was transferred to the genus Ruegeria as Ruegeria algicola, and has recently been reclassified within a novel genus and species, namely Marinovum algicola (Uchino et al., 1998; Martens et al., 2006). Roseobacter gallaeciensis has recently been reclassified within a novel genus, Phaeobacter, as Phaeobacter gallaeciensis (Martens et al., 2006). The genus Leisingera was proposed by Schaefer et al. (2002) with a single species, Leisingera methylohalidivorans. Comparative 16S rRNA gene sequence analyses have shown that the genus Leisingera is phylogenetically closely related to the genera Marinovum and Phaeobacter (Schaefer et al., 2002; Lee et al., 2005; Martens et al., 2006). Here we describe a bacterial strain, TF-218T, which is phylogenetically closely related to the genera Leisingera, Marinovum and Phaeobacter. The aim of the present study was to determine the exact taxonomic position of strain TF-218T by using a polyphasic characterization that included determination of the phenotypic and chemotaxonomic properties and a detailed phylogenetic analysis based on 16S rRNA gene sequences.
Strain TF-218T was isolated from a tidal flat sediment of the Yellow Sea, Korea, by means of the standard dilution plating technique at 25 °C on marine agar 2216 (MA; Difco). The type strains of P. gallaeciensis, Phaeobacter inhibens, L. methylohalidivorans and M. algicola were used as reference strains: P. gallaeciensis DSM 17395T, P. inhibens DSM 16374T, L. methylohalidivorans DSM 14336T and M. algicola DSM 10251T were obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany. The morphological, physiological and biochemical characteristics of strain TF-218T were investigated using routine cultivation on MA at 37 °C. The cell morphology was examined by using light microscopy (E600; Nikon) and transmission electron microscopy. The presence of flagella was determined using transmission electron microscopy with cells from exponentially growing cultures. For transmission electron microscopic observations, the cells were negatively stained with 1 % (w/v) phosphotungstic acid and the grids were examined, after being air-dried, with a Philips CM-20 transmission electron microscope. Growth under anaerobic conditions was determined after incubation in a Forma anaerobic chamber on MA and on MA supplemented with nitrate, both of which had been prepared anaerobically using nitrogen. Growth in the absence of NaCl was investigated by using trypticase soy broth prepared according to the formula of the Difco medium, except that no NaCl was used. Growth at various NaCl concentrations (0.5 and 1.0–10.0 %, w/v, using increments of 1.0 %) was investigated in marine broth 2216 (MB; Difco) or trypticase soy broth (Difco). Growth at various temperatures (4–50 °C) was measured on MA. Catalase and oxidase activities and the hydrolysis of casein, starch and Tweens 20, 40, 60 and 80 were determined as described by Cowan & Steel (1965). The hydrolysis of hypoxanthine, tyrosine and xanthine was tested on MA using the substrate concentrations described by Cowan & Steel (1965). The hydrolysis of aesculin, gelatin and urea and the reduction of nitrate were investigated as described previously (Lanyi, 1987), with the modification that artificial seawater was used for preparation of the media. The artificial seawater contained (l–1 distilled water) 23.6 g NaCl, 0.64 g KCl, 4.53 g MgCl2.6H2O, 5.94 g MgSO4.7H2O and 1.3 g CaCl2.2H2O (Bruns et al., 2001). H2S production was tested as described previously (Bruns et al., 2001). For in vivo pigment-absorption spectrum analysis, two strains were cultivated aerobically in the dark at 37 °C in liquid Erythromicrobium/Roseococcus medium (Yurkov et al., 1994; DSMZ medium no. 767) with the modification that D-glucose was used instead of acetate. The cultures were washed twice by centrifugation using a MOPS buffer (MOPS/NaOH, 0.01 M; KCl, 0.1 M; MgCl2, 0.001 M; pH 7.5) and disrupted by sonication with a Branson 450 sonifier. After the removal of cell debris by centrifugation, the absorption spectrum of the supernatant was examined on a Beckman Coulter DU800 spectrophotometer. Susceptibility to antibiotics was tested on MA plates by using antibiotic discs at the following concentrations: polymyxin B, 100 U; streptomycin, 50 µg; penicillin G, 20 U; chloramphenicol, 100 µg; ampicillin, 10 µg; cephalothin, 30 µg; gentamicin, 30 µg; novobiocin, 5 µg; tetracycline, 30 µg; kanamycin, 30 µg; lincomycin, 15 µg; oleandomycin, 15 µg; neomycin, 30 µg; and carbenicillin, 100 µg. Acid production from carbohydrates was tested as described by Leifson (1963). The utilization of various substrates for growth was determined as described by Baumann & Baumann (1981), using supplementation with 2 % (v/v) Hutner's mineral base (Cohen-Bazire et al., 1957) and 1 % (v/v) vitamin solution (Staley, 1968). Other physiological and biochemical tests were performed with the API 20E and API ZYM systems (bioMérieux).
Cell biomass of strain TF-218T for DNA extraction and for isoprenoid quinone and polar lipid analyses was obtained from cultures grown in MB at 37 °C. Cell biomass of P. gallaeciensis DSM 17395T and P. inhibens DSM 16374T for polar lipid analyses was obtained from cultures grown in MB at 25 and 28 °C, respectively. Chromosomal DNA was isolated and purified according to the method described by Yoon et al. (1996), with the exception that RNase T1 was used in combination with RNase A to minimize the contamination of RNA. The 16S rRNA gene was amplified by using a PCR with two universal primers, 5'-GAGTTTGATCCTGGCTCAG-3' and 5'-AGAAAGGAGGTGATCCAGCC-3', as described previously (Yoon et al., 1998). Sequencing of the amplified 16S rRNA gene and phylogenetic analysis were performed as described by Yoon et al. (2003). Isoprenoid quinones were analysed as described by Komagata & Suzuki (1987), using reversed-phase HPLC. For cellular fatty acid analysis, cell mass of strain TF-218T was harvested from MA plates after cultivation for 3 days at 37 °C; cell mass of P. gallaeciensis DSM 17395T, P. inhibens DSM 16374T, L. methylohalidivorans DSM 14336T and M. algicola DSM 10251T was harvested from MA plates after cultivation for 3 days at 25, 28, 25 and 28 °C, respectively. The fatty acids were extracted and fatty acid methyl esters were prepared according to the standard protocol of the MIDI/Hewlett Packard Microbial Identification System (Sasser, 1990). Polar lipids were extracted according to the procedures described by Minnikin et al. (1984) and identified by using two-dimensional TLC followed by spraying with appropriate detection reagents (Minnikin et al., 1984; Komagata & Suzuki, 1987). The presence of phosphatidylcholine was identified by spraying Dragendorff's reagent (Sigma). The DNA G+C content was determined by using the method of Tamaoka & Komagata (1984), with the modification that DNA was hydrolysed and the resultant nucleotides were analysed by using reversed-phase HPLC. DNA–DNA hybridization was performed fluorometrically according to the method of Ezaki et al. (1989), using photobiotin-labelled DNA probes and microdilution wells. Hybridization was performed with five replications for each sample: the highest and lowest values obtained for each sample were excluded and the means of the remaining three values were quoted as DNA–DNA relatedness values.
Morphological, cultural, physiological and biochemical characteristics of strain TF-218T are given in the species description (see below) or are shown in Table 1. The almost-complete 16S rRNA gene sequence of strain TF-218T determined in this study comprised 1419 nt, representing approximately 96 % of the Escherichia coli 16S rRNA gene sequence. Comparative 16S rRNA gene sequence analysis showed that strain TF-218T was most closely related phylogenetically to members of the genera Phaeobacter, Leisingera and Marinovum within the Alphaproteobacteria. In the phylogenetic tree obtained using the neighbour-joining algorithm, strain TF-218T formed part of the clade comprising two Phaeobacter species, with a bootstrap resampling value of 58.4 %, and this cluster was part of the lineage of L. methylohalidivorans, with a bootstrap resampling value of 88.9 % (Fig. 1). These phylogenetic relationships were also maintained in trees generated with the maximum-likelihood and maximum-parsimony algorithms (Fig. 1). Strain TF-218T exhibited 16S rRNA gene sequence similarity values of 97.5, 97.7, 97.3 and 96.3 % with respect to the type strains of P. gallaeciensis, P. inhibens, L. methylohalidivorans and M. algicola, respectively. The 16S rRNA gene sequence similarity values between strain TF-218T and other species used in the phylogenetic analysis were below 95.2 %. The predominant isoprenoid quinone detected in strain TF-218T was Q-10 (at a peak area ratio of approximately 94 %). The fatty acid profile of strain TF-218T comprised major amounts of unsaturated, straight-chain and hydroxy fatty acids and 11-methyl C18 : 17c; major fatty acids (>10 % of total fatty acids) were C18 : 17c (57.7 %) and 11-methyl-C18 : 17c (16.6 %) (Table 2). This fatty acid profile was similar to those of the type strains of P. gallaeciensis, P. inhibens, L. methylohalidivorans and M. algicola, although there were differences in the proportions of some fatty acids (Table 2). The major polar lipids detected in strain TF-218T were phosphatidylcholine, phosphatidylglycerol, phosphatidylethanolamine, two unidentified lipids and an aminolipid (Fig. 2). The DNA G+C content of strain TF-218T was 64.9 mol%.
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; Table 1
). Strain TF-218T can also be differentiated from M. algicola in view of the phylogenetic relationships among strain TF-218T and the genera Phaeobacter, Leisingera and Marinovum (Fig. 1). Accordingly, it was concluded that strain TF-218T is more closely affiliated to the members of the genus Phaeobacter than it is to those of the genera Leisingera and Marinovum or to a novel genus, on the basis of phylogenetic and chemotaxonomic relatedness (Martens et al., 2006; Fig. 1). Strain TF-218T exhibited mean DNA–DNA relatedness values of 15 and 18 % with respect to P. gallaeciensis DSM 17395T and P. inhibens DSM 16374T, respectively. These values indicate that strain TF-218T represents a genomic species that is distinct from the two Phaeobacter species (Wayne et al., 1987). Strain TF-218T can be clearly distinguished from the two recognized Phaeobacter species on the basis of differences in phenotypic properties, including colony pigmentation, nitrate reduction, utilization of several substrates and DNA G+C content (Table 1). On the basis of the data presented, strain TF-218T should be placed in the genus Phaeobacter as representing a novel species, for which the name Phaeobacter daeponensis sp. nov. is proposed.
Emended description of the genus Phaeobacter Martens et al. 2006
The description is as given by Martens et al. (2006), with the following amendments. On MA, colonies are brownish to dark brown or yellowish white; a diffusible brownish pigment is produced or not produced. Nitrate reduction is variable. The DNA G+C contents are in the range 55.7–64.9 mol%.
Description of Phaeobacter daeponensis sp. nov.
Phaeobacter daeponensis (dae.po.nen'sis. N.L. masc. adj. daeponensis of Daepo, Korea, where the type strain was isolated).
Cells are Gram-negative and oval (0.4–0.9x0.7–2.0 µm). Motile by means of single polar flagella. Colonies on MA are circular, slightly convex, smooth, glistening, yellowish white in colour and 1.5–2.5 mm in diameter after 3 days incubation at 37 °C. Growth occurs at 4 and 42 °C, but not at 43 °C. Optimal pH for growth is between 7.0 and 8.0; growth occurs at pH 5.5, but not at pH 5.0. Growth occurs in the presence of 8 % (w/v) NaCl, but not in the absence of NaCl or in the presence of more than 9 % (w/v) NaCl. Anaerobic growth does not occur on MA, but occurs on MA supplemented with nitrate. Catalase- and oxidase-positive. Bacteriochlorophyll a is absent. Hypoxanthine and L-tyrosine are hydrolysed, but aesculin, casein, xanthine and Tweens 20, 40 and 60 are not. Arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase and tryptophan deaminase are absent. In assays with the API ZYM system, alkaline phosphatase, esterase (C4), esterase lipase (C8), leucine arylamidase and acid phosphatase are present, but lipase (C14), valine arylamidase, cystine arylamidase, trypsin, 
-chymotrypsin, naphthol-AS-BI-phosphohydrolase, -galactosidase, 
-galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase are absent. L-Malate and pyruvate are utilized as carbon and energy sources, but benzoate, formate and salicin are not. Acid is produced from D-ribose, but not from L-arabinose, D-cellobiose, D-fructose, D-galactose, D-glucose, lactose, maltose, D-mannose, D-melezitose, melibiose, D-raffinose, L-rhamnose, sucrose, D-trehalose, D-xylose, myo-inositol, D-mannitol or D-sorbitol. Susceptible to ampicillin, carbenicillin, cephalothin, oleandomycin and polymyxin B, but not to lincomycin or tetracycline. The predominant ubiquinone is Q-10. The major fatty acids (>10 % of total fatty acids) are C18 : 17c and 11-methyl C18 : 17c. The major polar lipids are phosphatidylcholine, phosphatidylglycerol, phosphatidylethanolamine, two unidentified lipids and an aminolipid. The DNA G+C content of the type strain is 64.9 mol% (determined by HPLC). Other phenotypic characteristics are given in Table 1.
The type strain, TF-218T (=KCTC 12794T=JCM 13606T), was isolated from a tidal flat at Daepo Beach (Yellow Sea), Korea.
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ACKNOWLEDGEMENTS |
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