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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, Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
3 Department of Food and Life Science, Sungkyunkwan University, Chunchun-dong 300, Jangan-gu, Suwon, Korea
Correspondence
Yong-Ha Park
yhpark{at}kribb.re.kr
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7c and/or iso-C15 : 0 2OH, C16 : 0 and C18 : 1 7c as the major fatty acids, which are consistent with the corresponding data for Alteromonas macleodii. The DNA G+C contents of strains SW-47T and SW-49 were 45 and 44 mol%, respectively. Strains SW-47T and SW-49 showed a high level of 16S rDNA sequence similarity (99·9 %) and a mean level of DNA–DNA relatedness of 96·5 %. Phylogenetic analyses based on 16S rDNA sequences showed that the two strains form a coherent cluster with A. macleodii. Strains SW-47T and SW-49 exhibited levels of 16S rDNA sequence similarity of 99·3 and 99·1 %, respectively, with A. macleodii DSM 6062T and of less than 89·4 % with other species used in the phylogenetic analyses. Alteromonas fuliginea CIP 105339T was found to be more closely related to the genus Pseudoalteromonas than to the genus Alteromonas. On the basis of phenotypic properties and phylogenetic and genomic data, strains SW-47T and SW-49 represent a new species of the genus Alteromonas, for which the name Alteromonas marina (type strain SW-47T=KCCM 41638T=JCM 11804T) is proposed.
A light micrograph of strain SW-47T and a phylogenetic tree constructed using a larger dataset are available in IJSEM Online.
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and included four species, Alteromonas macleodii, Alteromonas communis, Alteromonas vaga and ‘Alteromonas marinopraesens’. Initially, the genus Alteromonas accommodated strictly aerobic, non-spore-forming, straight or curved rods that were motile by means of polar flagella (Baumann et al., 1972). There were at least 21 validly described species within the genus Alteromonas. However, the majority of these species have been reclassified in other genera, namely, Marinomonas, Pseudoalteromonas and Shewanella (Coyne et al., 1989; Gauthier et al., 1995; Ivanova et al., 2000, 2001; MacDonell & Colwell, 1985; Sawabe et al., 2000; van Landschoot & De Ley, 1983). There are two validly described Alteromonas species, A. macleodii (Baumann et al., 1972) and Alteromonas fuliginea (Romanenko et al., 1994), at the time of writing. Phylogenetic analyses based on 16S rDNA sequence data showed that A. macleodii falls within the 
-subgroup of the class Proteobacteria (Anzai et al., 2000). Recently, we isolated two moderately halophilic bacterial strains, SW-47T and SW-49, from the East Sea in Korea. The bacteria were considered to be Alteromonas-like organisms as a result of a 16S rDNA sequence comparison. Accordingly, the aim of the present work was to establish the exact taxonomic positions of strains SW-47T and SW-49, using a combination of phenotypic characterization, detailed phylogenetic analyses (based on 16S rDNA sequences) and genomic relatedness. In this study, the type strain of A. fuliginea, the 16S rDNA sequence of which has not been determined before, was subjected to 16S rDNA sequencing and then analysed phylogenetically.
Strains SW-47T and SW-49 were isolated by the dilution-plating technique on marine agar 2216 (MA) (Difco). Cell biomass of strains SW-47T and SW-49 and A. macleodii DSM 6062T for respiratory lipoquinone analysis and for DNA extraction was obtained from cultures in marine broth 2216 (MB) (Difco) at 30 °C. Cell biomass of A. fuliginea CIP 105339T was produced in MB at 30 °C. All strains were cultivated on a gyratory shaker at 150 r.p.m. For fatty acid methyl ester (FAME) analysis, cell mass of strains SW-47T and SW-49 and A. macleodii DSM 6062T was obtained from agar plates after cultivation for 3 days at 30 °C on MA. A. macleodii DSM 6062T was obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany, and A. fuliginea CIP 105339T was obtained from the Collection de l'Institut Pasteur (CIP), Paris, France. Cell morphology was examined by light microscopy (Nikon E600) and transmission electron microscopy (TEM). Flagellation was examined using TEM with cells from exponentially growing cultures. The cells were negatively stained with 1 % (w/v) phosphotungstic acid and, after air-drying, the grids were examined by using a model CM-20 transmission electron microscope (Philips). Gram reaction was determined using the bioMérieux Gram Stain kit according to the manufacturer's instructions. Growth at various NaCl concentrations was investigated after 14 days incubation in MB. Growth at various temperatures was investigated after 14 days incubation on MA at 4–50 °C. Growth under anaerobic conditions was determined after incubation for 28 days in an anaerobic chamber with MA that had been prepared anaerobically using nitrogen. Catalase and oxidase activities and hydrolysis of casein and starch were determined as described by Cowan & Steel (1965). Hydrolysis of aesculin was determined according to the method of Lanyi (1987), with the addition of 3 % (w/v) NaCl. Hydrolysis of hypoxanthine, tyrosine, xanthine and Tween 80 was tested on MA plates with the substrate concentrations described previously (Cowan & Steel, 1965). Hydrolysis of gelatin and nitrate reduction were studied as described previously (Cowan & Steel, 1965) with a modification that artificial sea water (Levring, 1946) was used. Hydrolysis of birchwood xylan (Sigma) was tested on solid marine salts basal medium (Baumann & Baumann, 1981) supplemented with 0·5 % (w/v) xylan as sole carbon source. H2S production was tested as described previously (Bruns et al., 2001). Utilization of substrates as sole carbon and energy sources was tested as described by Baumann & Baumann (1981). Acid production from carbohydrates was determined according to Leifson (1963). Enzyme activity was determined by using the API ZYM system (bioMérieux).
Respiratory lipoquinones were analysed as described previously (Komagata & Suzuki, 1987) using reversed-phase HPLC. For quantitative analysis of cellular fatty acid compositions, a loopful of a culture grown on MA was harvested and FAMEs were extracted and prepared by the standard protocol of the MIDI/Hewlett Packard Microbial Identification System (Sasser, 1990). Chromosomal DNA was isolated and purified according to the method described previously (Yoon et al., 1996), except that ribonuclease T1 was used with ribonuclease A. The G+C content of the DNA 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 as described previously (Yoon et al., 1998). The PCR product was purified with a QIAquick PCR purification kit (Qiagen). Sequencing of the purified 16S rDNA PCR product was performed as described previously (Yoon et al., 2003). 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 analyses. Phylogenetic trees were inferred by using three different calculation methods, i.e. the neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Kluge & Farris, 1969) algorithms implemented in the PHYLIP software package version 3.5 (Felsenstein, 1993). Evolutionary distance matrices for the neighbour-joining method were calculated with the algorithm of Jukes & Cantor (1969) with the DNADIST program. The stability of grouping was assessed by a bootstrap analysis based on 1000 resamplings of the neighbour-joining dataset by using the programs SEQBOOT, DNADIST, NEIGHBOR and CONSENSE of the PHYLIP software 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. Of the values obtained, the highest and lowest values in each sample were excluded and the remaining three values were used for calculation of the similarity values. DNA relatedness values are the mean of three values.
Strains SW-47T and SW-49 were Gram-negative, non-spore-forming bacteria. Cells of the two strains were rod-shaped, measuring approximately 1·0–1·2 µm in width by 2·5–4·0 µm in length after 3 days cultivation at 30 °C on MA. The two strains were motile by means of a single polar flagellum [a light micrograph of strain SW-47T is available as supplementary data in IJSEM Online (http://ijs.sgmjournals.org)]. Colonies on MA were circular, smooth, raised and cream in colour and 2·0–3·0 mm in diameter after incubation for 2 days at 30 °C. Strains SW-47T and SW-49 grew optimally at 30–37 °C; they grew at 4 °C and their maximum growth temperature was 44 °C. The strains grew well over a broad pH range, pH 5·5–9·0, with an optimum between pH 7·0 and 8·0; they grew at pH 5·0 but not at pH 4·5. Both strains grew optimally in the presence of 2–5 % (w/v) NaCl and did not grow without NaCl or in the presence of >15 % NaCl. The two strains did not grow under anaerobic conditions on MA. Strains SW-47T and SW-49 showed catalase and oxidase activities but no urease activity. Aesculin, casein, gelatin, hypoxanthine, starch, Tween 80 and tyrosine were hydrolysed, but xanthine and xylan were not. H2S was not produced and nitrate was not reduced to nitrite or nitrogen. The following enzymes were present in strains SW-47T and SW-49, when assayed using the API ZYM system: alkaline phosphatase, esterase (C4), esterase lipase (C8), lipase (C14), acid phosphatase and naphthol-AS-BI-phosphohydrolase. Results for utilization of and acid production from different substrates are shown in Table 1 or are given in the species description (see below). The phenotypic properties of strains SW-47T and SW-49 are summarized in Table 1, together with those of A. macleodii. As shown in Table 1, there are differences between strains SW-47T and SW-49 and A. macleodii in some characteristics.
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). Strains SW-47T and SW-49 contained C16 : 1 7c and/or iso-C15 : 0 2OH, C16 : 0 and C18 : 1 7c as the major fatty acids (Table 2). These fatty acid profiles were similar to that of A. macleodii DSM 6062T (Table 2). A similar fatty acid pattern for the type strain of A. macleodii was reported by Svetashev et al. (1995). However, there are differences in the proportion of fatty acids between this study and the study of Svetashev et al. (1995), which may be caused by different cultivation, extraction or analytical conditions. The DNA G+C contents of strains SW-47T and SW-49 were 45 and 44 mol%, respectively.
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; a phylogenetic tree constructed using a larger dataset is available in IJSEM Online (http://ijs.sgmjournals.org)]. This cluster joined to the evolutionary lineage of A. macleodii, and this relationship was supported by a bootstrap value of 100 % (Fig. 1). This tree topology was also found in the trees generated with the maximum-likelihood and maximum-parsimony algorithms (data not shown). Strains SW-47T and SW-49 exhibited levels of 16S rDNA similarity of 99·3 and 99·1 %, respectively, with A. macleodii DSM 6062T (Fig. 1). Sequence similarities to all other taxa included in the phylogenetic analyses were less than 89·4 % (Fig. 1). A. fuliginea CIP 105339T was found to be phylogenetically only distantly related to A. macleodii DSM 6062T and strains SW-47T and SW-49, and formed a phylogenetic lineage within the radiation of the cluster comprising Pseudoalteromonas species. A. fuliginea CIP 105339T showed levels of 16S rDNA similarity of 89·0–89·1 % to A. macleodii DSM 6062T and strains SW-47T and SW-49. Sequence similarity values between A. fuliginea CIP 105339T and the type strains of Pseudoalteromonas species were 91·2–99·7 %. A. fuliginea CIP 105339T showed high levels of 16S rDNA similarity, of 98·5–99·7 %, with organisms in the clade including Pseudoalteromonas haloplanktis. Therefore, A. fuliginea may have to be reclassified as a member of the genus Pseudoalteromonas through additional taxonomic study.
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).
In view of the results from the morphological, chemotaxonomic and phylogenetic analyses done in this study, it is appropriate that strains SW-46T and SW-52 be classified in the genus Alteromonas. The level of DNA–DNA relatedness, together with differential phenotypic properties and phylogenetic data, justify a taxonomic discrimination of strains SW-47T and SW-49 from A. macleodii (Wayne et al., 1987). Therefore, on the basis of the data presented here, strains SW-46T and SW-52 should be placed in the genus Alteromonas as members of a novel species, for which we propose the name Alteromonas marina.
Description of Alteromonas marina sp. nov.
Alteromonas marina (ma.ri'na. L. fem. adj. marina of the sea, marine).
Cells are rod-shaped, measuring 1·0–1·2 µm in width and 2·5–4·0 µm in length when grown on MA. Gram-negative. Non-spore-forming. Motile by means of a single polar flagellum. Colonies on MA are circular, smooth, raised and cream-coloured and 2·0–3·0 mm in diameter after 2 days incubation at 30 °C. The optimal temperature for growth is 30–37 °C. Growth occurs at 4 and 44 °C but not above 45 °C. The optimal pH for growth is between pH 7·0 and 8·0. Growth is observed at pH 5·0 but not at pH 4·5. Optimal growth occurs in the presence of 2–5 % (w/v) NaCl. No growth occurs in the absence of NaCl or in the presence of more than 15 % NaCl. Growth does not occur under anaerobic conditions on MA. Catalase- and oxidase-positive. Urease-negative. Aesculin, casein, hypoxanthine and tyrosine are hydrolysed. Xanthine and xylan are not hydrolysed. H2S is not produced. When assayed with the API ZYM system, alkaline phosphatase, esterase (C4), esterase lipase (C8), lipase (C14), acid phosphatase and naphthol-AS-BI-phosphohydrolase are present, but cysteine arylamidase, trypsin, 
-chymotrypsin, -galactosidase, 
-galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase are absent. Other characteristics are given in Table 1
. The predominant respiratory lipoquinone is ubiquinone-8 (Q-8). The major fatty acids are C16 : 1 7c and/or iso-C15 : 0 2OH 16 : 0, C16 : 0 and C18 : 1 7c. DNA G+C content is 44–45 mol% (HPLC). Isolated from sea water of Hwajinpo beach of the East Sea in Korea. Reference strain is SW-49 (=KCCM 41639=JCM 11805).
The type strain is SW-47T (=KCCM 41638T=JCM 11804T). Its G+C content is 45 mol%.
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ACKNOWLEDGEMENTS |
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