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1 Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
2 National Research Laboratory of Molecular Ecosystematics, Institute of Probionic, Probionic Corporation, Bio-venture Center, KRIBB, PO Box 115, Yusong, Taejon, Korea
Correspondence
Jung-Hoon Yoon
jhyoon{at}kribb.re.kr
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9c were also present. The DNA G+C content of strain TF-17T was 59·9 mol%. Levels of DNA–DNA relatedness between strain TF-17T and the type strains of the three Microbulbifer species were in the range 10·0–13·0 %. On the basis of phenotypic and phylogenetic data and genotypic distinctiveness, strain TF-17T (=KCCM 41774T=JCM 12187T) is proposed as the type strain of a novel species of the genus Microbulbifer, Microbulbifer maritimus sp. nov.
Published online ahead of print on 23 January 2004 as DOI 10.1099/ijs.0.02985-0.
The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain TF-17T is AY377986.
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for a novel rod-shaped and strictly aerobic marine bacterium that belonged to the Proteobacteria. A single species, Microbulbifer hydrolyticus, was included within this genus. The second species of the genus Microbulbifer was Microbulbifer salipaludis, which was proposed recently by Yoon et al. (2003b). Phylogenetic analyses based on 16S rDNA sequences have shown that the two Microbulbifer species fall within the 
-subclass of the Proteobacteria (González et al., 1997; Solano & Sanchez-Amat, 1999; Anzai et al., 2000; Yoon et al., 2003b). Chemical markers of this genus include the presence of a major amount of iso-C15 : 0 and ubiquinone with eight isoprene units (Q-8) (González et al., 1997; Yoon et al., 2003b). The DNA G+C content of the genus is 58–59 mol% (González et al., 1997; Yoon et al., 2003b). Pigmentation of the colonies of these two Microbulbifer species is cream or greyish-yellow. Recently, Pseudomonas elongata was transferred to the genus Microbulbifer as Microbulbifer elongatus (Yoon et al., 2003a). The colour of M. elongatus was yellowish-brown, unlike the first two Microbulbifer species that were described. In the course of screening taxonomically useful micro-organisms that were present in an intertidal sediment from the Yellow Sea (Korea), a yellowish brown-coloured, slightly halophilic bacterial strain (TF-17T) was isolated and characterized taxonomically. The result of 16S rDNA sequence comparison indicated that this isolate is related phylogenetically to members of the genus Microbulbifer. Accordingly, the aim of this work was to establish the exact taxonomic position of strain TF-17T by polyphasic characterization, which included phenotypic properties, detailed phylogenetic analysis based on 16S rDNA sequences and genomic relatedness.
Strain TF-17T was isolated by the dilution-plating technique on marine agar 2216 (MA; Difco). Cell biomass of strain TF-17T for respiratory lipoquinone analysis and for DNA extraction was obtained from cultures in marine broth 2216 (MB; Difco) at 37 °C. For fatty acid methyl ester analysis, cell mass of strain TF-17T was obtained from agar plates after incubation for 3 days at 37 °C on MA. Cell morphology was examined by light microscopy and transmission electron microscopy (TEM). Flagellum type was examined by TEM using cells from an exponentially growing culture. Gram-reaction was determined by using a Gram Stain kit (bioMérieux) according to the manufacturer's instructions. Growth under anaerobic conditions was determined after incubation in an anaerobic chamber with anaerobically prepared MA. Growth in the absence of NaCl was investigated in trypticase soy broth to which NaCl was not added. Growth at various NaCl concentrations (0·5–15 %) was investigated in MB or in trypticase soy broth. Growth at various temperatures (4–55 °C) was measured on MA. Catalase activity was determined by bubble production in 3 % (v/v) H2O2 solution. Oxidase activity was determined by oxidation of 1 % p-aminodimethylaniline oxalate. Hydrolysis of gelatin and aesculin and nitrate reduction were determined as described by Lanyi (1987), with the modification that artificial sea water was used. Artificial sea water contained [(l distilled water)–1]: 23·6 g NaCl; 0·64 g KCl; 4·53 g MgCl2.6H2O; 5·94 g MgSO4.7H2O; 1·3 g CaCl2.2H2O (Levring, 1946). Hydrolysis of casein and starch was determined as described by Cowan & Steel (1965). Hydrolysis of hypoxanthine, tyrosine, xanthine and Tween 80 was tested on MA plates by using substrate concentrations that were described by Cowan & Steel (1965). Hydrolysis of chitin (Sigma) and birchwood xylan (Sigma) was determined on solid and in liquid marine salts basal medium (Baumann & Baumann, 1981) that contained 0·5 % chitin or xylan as the sole carbon source, respectively. M. hydrolyticus DSM 11525T was used as positive control for hydrolysis tests of chitin and xylan. Additional enzyme activity was determined by using the API ZYM system (bioMérieux). Acid production from carbohydrates was determined as described by Leifson (1963). Utilization of various substrates for growth was determined as described by Yurkov et al. (1994).
Chromosomal DNA was isolated and purified according to a method described previously (Yoon et al., 1996), except that ribonuclease T1 was used together with ribonuclease A. Respiratory lipoquinones were analysed as described by Komagata & Suzuki (1987), using reversed-phase HPLC. For quantitative analysis of cellular fatty acid compositions, a loop of cell mass was harvested and fatty acid methyl esters were prepared and identified by following the instructions of the Microbial Identification system (MIDI). DNA G+C content was determined by the method of Tamaoka & Komagata (1984). DNA was hydrolysed and the resultant nucleotides were analysed by reversed-phase HPLC.
16S rDNA was amplified by PCR using two universal primers (Yoon et al., 1998). The PCR product was purified with a QIAquick PCR purification kit (Qiagen). Sequencing of the purified 16S rDNA was performed by using an ABI PRISM BigDye Terminator cycle sequencing ready reaction kit (Applied Biosystems) as recommended by the manufacturer. The purified sequencing reaction mixtures were electrophoresed automatically on an Applied Biosystems model 377 automatic DNA sequencer. Alignment of sequences was carried out with CLUSTAL W software (Thompson et al., 1994). Gaps at the 5' and 3' ends of the alignment were omitted from further analysis. Phylogenetic trees were inferred by using three tree-making algorithms: the neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Kluge & Farris, 1969) methods, implemented within the PHYLIP package (Felsenstein, 1993). Evolutionary distance matrices for the neighbour-joining method were calculated according to Jukes & Cantor (1969) by using the program DNADIST in the PHYLIP package. Stability of relationships was assessed by a bootstrap analysis based on 1000 resamplings of the neighbour-joining dataset, using the programs SEQBOOT, DNADIST, NEIGHBOR and CONSENSE of the PHYLIP package. DNA–DNA hybridization was performed fluorometrically by 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 remaining three values were used to calculate similarity values. DNA–DNA relatedness values quoted are the means of these three values.
Cells of strain TF-17T were rods that measured approximately 0·3–0·5 µm in width and 3·0–6·0 µm in length after cultivation for 3 days at 37 °C on MA. Strain TF-17T had no flagella. Colonies on MA were yellowish-brown in colour, smooth, irregular, slightly raised and 2·0–4·0 mm in diameter after 3 days incubation at 37 °C on MA. Strain TF-17T grew optimally at 37 °C, pH 6·5–7·5 and in the presence of 2–4 % (w/v) NaCl. Strain TF-17T did not grow under anaerobic conditions on MA. Phenotypic properties of strain TF-17T are shown in Table 1 or are given in the species description (see below). As shown in Table 1, there are differences between TF-17T and the other Microbulbifer species in some phenotypic characteristics.
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9c (Table 2). This profile was similar to those of the type strains of M. hydrolyticus, M. salipaludis and M. elongatus, although there are differences in the proportions of some fatty acids, such as iso-C11 : 0, iso-C11 : 0 3-OH and C18 : 17c. The DNA G+C content of strain TF-17T was 59·9 mol%.
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-subclass of the Proteobacteria and, in particular, to the genus Microbulbifer. In the phylogenetic tree based on the neighbour-joining algorithm, strain TF-17T clustered with the type strains of M. hydrolyticus, M. salipaludis and M. elongatus (Fig. 1). The relationship between strain TF-17T and the clade comprising the type strains of the three Microbulbifer species was supported by bootstrap analysis at a confidence level of 100 %. Similar tree topologies were generated by the maximum-parsimony method (data not shown). Strain TF-17T showed 16S rDNA sequence similarity levels of 95·1, 95·7 and 95·3 % to M. hydrolyticus ATCC 700072T, M. salipaludis KCCM 41586T and M. elongatus DSM 6810T, respectively. Sequence similarities to all other taxa included in the phylogenetic analysis were <90·5 % (Fig. 1). DNA–DNA hybridization was performed to determine genotypic relatedness between strain TF-17T and the type strains of the three Microbulbifer species. Strain TF-17T exhibited DNA–DNA relatedness levels of 11·5, 10·0 and 13·0 % to M. hydrolyticus DSM 11525T, M. salipaludis KCCM 41586T and M. elongatus DSM 6810T, respectively.
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, b). In particular, the predominant respiratory lipoquinone type and cellular fatty acid profile are useful for distinguishing strain TF-17T and other members of the genus Microbulbifer from some other related genera. Strain TF-17T and other members of the genus Microbulbifer contain Q-8 as the predominant respiratory lipoquinone (Yoon et al., 2003a, b), whereas members of the genus Marinobacter and authentic pseudomonads have been known to contain Q-9 as the predominant respiratory lipoquinone (Oyaizu & Komagata, 1983; Yumoto et al., 2001; Yoon et al., 2003a). Strain TF-17T can be distinguished from members of the genus Alcanivorax by cellular fatty acid profiles: strain TF-17T and other members of the genus Microbulbifer contain iso-C15 : 0 as the major fatty acid, whereas members of the genus Alcanivorax contain C18 : 17c and C16 : 0 as the major fatty acids (Fernández-Martínez et al., 2003). Therefore, both phylogenetic and chemotaxonomic results indicate clearly that strain TF-17T belongs to the genus Microbulbifer.
Although strain TF-17T is similar to M. elongatus in its morphological properties, it is differentiated from M. elongatus in some physiological properties (Table 1
). There are some noteworthy differences between strain TF-17T and the other two Microbulbifer species in morphological, physiological and biochemical properties, including colour of colonies, maximum growth temperature, ability to hydrolyse some substrates and acid production from carbohydrates (Table 1). Levels of 16S rDNA similarity between strain TF-17T and the type strains of Microbulbifer species (95·1–95·7 %) are low enough to exclude the possibility of assigning strain TF-17T to a previously described Microbulbifer species (Stackebrandt & Goebel, 1994). In addition, DNA–DNA relatedness levels justify that strain TF-17T is separate from the three Microbulbifer species with validly published names (Wayne et al., 1987). Therefore, on the basis of phenotypic, chemotaxonomic and phylogenetic data and genotypic distinctiveness, strain TF-17T should be placed in the genus Microbulbifer as the type strain of a novel species, for which we propose the name Microbulbifer maritimus sp. nov.
Description of Microbulbifer maritimus sp. nov.
Microbulbifer maritimus (ma.ri.ti'mus. L. masc. adj. maritimus living near the sea).
Cells are rods, 0·3–0·5 µm wide and 3·0–6·0 µm long. Gram-negative. Colonies on MA are yellowish-brown in colour, smooth, irregular, slightly raised and 2·0–4·0 mm in diameter after 3 days incubation at 37 °C. Optimal growth temperature is 37 °C. Growth occurs at 15 and 48 °C, but not at 10 °C or above 49 °C. Optimal growth pH is 6·5–7·5. Growth occurs weakly at pH 5·0, but not at pH 4·5. Optimal growth occurs in the presence of 2–4 % NaCl. Growth occurs in the presence of 10 % NaCl, but not without NaCl or in the presence of >11 % NaCl. No growth occurs under anaerobic conditions on MA. Predominant respiratory lipoquinone is Q-8. Major fatty acid is iso-C15 : 0 and significant amounts of iso-C11 : 0 3-OH and iso-C17 : 19c are also present. DNA G+C content is 59·9 mol% (determined by HPLC). Tyrosine is hydrolysed, but hypoxanthine, xanthine and xylan are not. Acid is not produced from adonitol, myo-inositol, D-mannitol, D-melezitose, melibiose, D-raffinose, L-rhamnose, D-ribose, D-sorbitol or stachyose. D-Glucose, D-cellobiose, L-arginine, L-serine, acetate, butyrate, DL-malate, pyruvate and succinate are utilized for growth. D-Fructose, lactose, mannose, sucrose, hexadecane, mannitol, ethanol, methanol, benzoate, citrate, formate, DL-glutamate and lactate are not utilized. The following enzymes are present when assayed with the API ZYM system: alkaline phosphatase, esterase (C4), lipase (C8), leucine arylamidase, acid phosphatase and naphthol-AS-BI-phosphohydrolase. The following enzymes are absent when assayed with the API ZYM system: lipase (C14), valine arylamidase, cystine arylamidase, trypsin, 
-chymotrypsin, -galactosidase, 
-galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase. Other phenotypic properties are given in Table 1.
The type strain is TF-17T (=KCCM 41774T=JCM 12187T), which was isolated from an intertidal sediment from the Yellow Sea, Korea.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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