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1 Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
2 The Center for Traditional Microorganism Resources, Keimyung University, Shindang-Dong, Dalseo-gu, Daegu, Korea
Correspondence
Jung-Hoon Yoon
jhyoon{at}kribb.re.kr
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains SW-117T and SW-120T and Shewanella colwelliana ATCC 39565T are AY485224, AY485225 and AY653177, respectively.
Detailed phenotypic characteristics of Shewanella marisflavi, Shewanella aquimarina and related species, and an expanded neighbour-joining tree are available as supplementary material in IJSEM Online.
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with two species that had been assigned to the genus Alteromonas, Alteromonas putrefaciens and Alteromonas hanedai. Subsequently, many Shewanella species have been isolated from a variety of sources, including aquatic and marine environments (Nealson et al., 1991; Ivanova et al., 2001; Bozal et al., 2002), clinical samples (Nozue et al., 1992; Brink et al., 1995; Venkateswaran et al., 1999), sediments (Myers & Nealson, 1988), oilfield fluids (Semple & Westlake, 1987) and others. The genus Shewanella is phylogenetically affiliated to the 
-Proteobacteria (Anzai et al., 2000). There are at least 25 recognized Shewanella species at the time of writing. In this study, we describe two Gram-negative, slightly halophilic, rod-shaped organisms, strains SW-117T and SW-120T, which were isolated from sea water of the Yellow Sea in Korea. From 16S rRNA gene sequence comparisons, these organisms were considered to be phylogenetically related to the genus Shewanella. Accordingly, the aim of the present work was to establish the taxonomic positions of strains SW-117T and SW-120T by using a combination of polyphasic taxonomic data.
Strains SW-117T and SW-120T were isolated by a standard dilution plating technique on marine agar 2216 (MA; Difco) at 30 °C. Shewanella marinintestina JCM 11558T, Shewanella sairae JCM 11563T and Shewanella schlegeliana JCM 11561T were obtained from the Japan Collection of Microorganisms (JCM), Saitama, Japan. Shewanella affinis KMM 3587T and Shewanella waksmanii KMM 3823T were obtained from Professor Elena P. Ivanova, Industrial Research Institute, Swinburne University of Technology, Australia. Shewanella colwelliana ATCC 39565T was obtained from the American Type Culture Collection (ATCC), Manassas, USA. Cell biomass of strains SW-117T and SW-120T for respiratory lipoquinone analysis and for DNA extraction was obtained from cultivation in marine broth 2216 (MB; Difco) at 30 °C. For fatty acid methyl ester (FAME) analysis, cell mass of strains SW-117T and SW-120T was obtained from agar plates after cultivation for 2 days at 30 °C on MA and trypticase soy agar (TSA; Difco). Cell morphology was examined by light microscopy (Nikon E600) and transmission electron microscopy (TEM). Flagellum type was examined by TEM using cells from exponentially growing cultures. Gram reaction was determined using a Gram Strain kit (bioMérieux) according to the manufacturer's instructions. The pH range for growth was determined in MB that was adjusted to various pH values (pH 4·5–9·0 at intervals of 0·5 pH units). Growth at various NaCl concentrations was investigated in MB or trypticase soy broth (Difco). Growth in the absence of NaCl was investigated in trypticase soy broth without NaCl. Growth at various temperatures (4–50 °C) was measured on MA. Growth under anaerobic conditions was determined after incubation in an anaerobic chamber on anaerobically prepared MA. Catalase activity was determined by bubble production in a 3 % (v/v) hydrogen peroxide solution. Oxidase activity was determined by oxidation of 1 % (w/v) p-aminodimethylaniline oxalate. Hydrolysis of casein, starch and Tween 80 was determined as described by Cowan & Steel (1965). Hydrolysis of hypoxanthine, tyrosine and xanthine was performed on MA using substrate concentrations described by Cowan & Steel (1965). Hydrolysis of gelatin and aesculin and nitrate reduction were determined as described by Lanyi (1987) with a modification that artificial sea water was used. The artificial sea water contained (per litre of 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 (Levring, 1946). Hydrolysis of birchwood xylan (Sigma) was determined on solid marine salts basal medium (Baumann & Baumann, 1981) containing 0·5 % (w/v) xylan as the sole carbon source. H2S production was tested as described by Bruns et al. (2001). Haemolytic activity was recorded on MA with 5 % defibrinated sheep blood. Enzyme activity was determined using the API ZYM system (bioMérieux). Acid production from carbohydrates was determined as described by Leifson (1963). Utilization of substrates as sole carbon and energy sources was tested as described by Baumann & Baumann (1981).
Isoprenoid quinones were extracted and analysed as described by Komagata & Suzuki (1987) using reversed-phase HPLC. For quantitative analysis of the cellular fatty acid compositions, a loop of cell mass was harvested and FAMEs were extracted and prepared according to the standard protocol of the MIDI/Hewlett Packard Microbial Identification System (Sasser, 1990). Chromosomal DNA was isolated and purified according to the method described by Yoon et al. (1996), except that ribonuclease T1 was used with ribonuclease A. The 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. The 16S rRNA gene was amplified by PCR using two universal primers as described by Yoon et al. (1998). Sequencing of the amplified 16S rRNA gene and phylogenetic analysis were performed as described by Yoon et al. (2003). 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; reported DNA–DNA relatedness values are the mean of the remaining three values.
Morphological, cultural, physiological and biochemical characteristics of strains SW-117T and SW-120T are shown in Table 1 or are given in the species descriptions below. Strain SW-117T grew at 4 °C and without NaCl, but strain SW-120T did not. Starch was hydrolysed by strain SW-120T, but not by strain SW-117T. D-Galactose was utilized by strain SW-120T, but not by strain SW-117T. Acid from D-glucose, D-cellobiose and maltose was produced by strain SW-117T, but not by strain SW-120T. Strains SW-117T and SW-120T contained simultaneously both menaquinones (MK) and ubiquinones (Q) as isoprenoid quinones. The predominant ubiquinones detected in strain SW-117T were Q-7 and Q-8 at a peak area ratio of about 49 and 48 %, respectively, and the predominant ubiquinones detected in strain SW-120T were Q-7 (67 %) and Q-8 (31 %). The two strains contained MK-7 as the predominant menaquinone (about 92 and 86 %, respectively). Strains SW-117T and SW-120T had cellular fatty acid profiles that contained large amounts of straight-chain, branched, unsaturated and hydroxy fatty acids (Table 2). There were differences in the proportions of some fatty acids when the two strains were grown on MA and TSA (Table 2). Strains SW-117T and SW-120T contained iso-C15 : 0, iso-C15 : 0 2-OH and/or C16 : 1
7c and C16 : 0 as the major fatty acids when they were grown on MA (Table 2). The proportions of iso-C15 : 0 2-OH and/or C16 : 17c and C16 : 0 decreased when the two strains were grown on TSA (Table 2). The proportions of some fatty acids, for example iso-C13 : 0, iso-C17 : 0 and iso-C13 : 0 3-OH, increased when the strains were grown on TSA (Table 2). The DNA G+C contents of strains SW-117T and SW-120T were 51 and 54 mol%, respectively, values higher than those of most Shewanella species (Table S1, supplementary table in IJSEM Online).
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). The relationship between this clade and the cluster comprising other Shewanella species was supported by a high bootstrap confidence level of 99·9 % (Fig. 1). The level of 16S rRNA gene sequence similarity between strains SW-117T and SW-120T was 97·4 %. Strains SW-117T and SW-120T exhibited highest 16S rRNA gene sequence similarity values to S. affinis KMM 3587T and S. colwelliana ATCC 39565T (98·5 %, respectively) and S. waksmanii KMM 3823T (97·0 %) (Fig. 1). Strains SW-117T and SW-120T exhibited 16S rRNA gene sequence similarity levels of 93·8–97·9 and 92·4–96·9 %, respectively, to the type strains of the other recognized Shewanella species. Levels of 16S rRNA gene sequence similarity between strains SW-117T and SW-120T and other species used in the phylogenetic analysis were lower than 91·9 % (Fig. 1). DNA–DNA hybridization was performed to determine the genetic relatedness between strains SW-117T and SW-120T, between strain SW-120T and the type strains of three Shewanella species, and between strain SW-117T and the type strains of six Shewanella species that showed 16S rRNA gene sequence similarity levels of more than 97 % to strain SW-117T. Strains SW-117T and SW-120T exhibited mean DNA–DNA relatedness of 10·1 %, when their DNAs were used individually as labelled DNA probes for cross-hybridization. This value indicates that strains SW-117T and SW-120T are members of different genomic species. Strain SW-117T exhibited DNA–DNA relatedness levels of 8·3–20·3 % to S. affinis KMM 3587T, S. colwelliana ATCC 39565T, S. waksmanii KMM 3823T, S. marinintestina JCM 11558T, S. sairae JCM 11563T and S. schlegeliana JCM 11561T. Strain SW-120T exhibited DNA–DNA relatedness levels of 6·3–13·7 % to S. affinis KMM 3587T, S. colwelliana ATCC 39565T and S. waksmanii KMM 3823T.
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-Proteobacteria, particularly to the genus Shewanella (Fig. 1
). The results obtained in chemotaxonomic analyses are consistent with the results of 16S rRNA gene sequence analysis and phylogenetic inference. The cellular fatty acid profiles of the two strains are similar to those of recognized Shewanella species, although there are some differences in the proportions of the major fatty acids (Bowman et al., 1997; Venkateswaran et al., 1999; Bozal et al., 2002; Ivanova et al., 2003a, b; Satomi et al., 2003). Strains SW-117T and SW-120T have respiratory lipoquinone patterns similar to those of Shewanella species, containing Q-7 and Q-8 as the predominant ubiquinones. Menaquinone detected in strain SW-117T and SW-120T has also been detected in some Shewanella species together with ubiquinones, although their compositions are variable for different strains or species (Nogi et al., 1998; Venkateswaran et al., 1999; Bozal et al., 2002).
Strains SW-117T and SW-120T have approximately 39 bp (2·6 %) differences between their 16S rRNA gene sequences. Both strains are considered to be members of different species based on DNA–DNA hybridization data, together with differences in the DNA G+C contents and in their phenotypic properties, including, among others, growth at 4 °C and in the absence of NaCl, and starch hydrolysis (Table 1). Strains SW-117T and SW-120T are differentiated from phylogenetically related Shewanella species by some physiological and biochemical characteristics, such as temperature for growth, NaCl tolerance and the ability to utilize certain substrates (Table 1 and Table S1 in IJSEM Online). Strain SW-117T exhibited 16S rRNA gene sequence similarity levels of less than 96·3 % to the type strains of other Shewanella species except S. affinis, S. colwelliana, S. waksmanii, S. marinintestina, S. sairae and S. schlegeliana. Levels of DNA–DNA relatedness between strains SW-117T and SW-120T and the type strains of some phylogenetically related Shewanella species are far below the threshold value (70 %) suggested for species delineation in current bacterial systematics (Wayne et al., 1987). Levels of 16S rRNA gene sequence similarity (92·4–97·0 %) between strain SW-120T and the type strains of Shewanella species are low enough to categorize strain SW-120T as representing a species distinct from recognized Shewanella species (Stackebrandt & Goebel, 1994). Therefore, in view of the combined phenotypic, chemotaxonomic and phylogenetic data, together with genomic distinctiveness, strains SW-117T and SW-120T should be placed in the genus Shewanella as two distinct novel species, for which the names Shewanella marisflavi sp. nov. and Shewanella aquimarina sp. nov. are proposed, respectively.
Description of Shewanella marisflavi sp. nov.
Shewanella marisflavi (ma.ris.fla'vi. L. gen. neut. n. maris of the sea; L. masc. adj. flavus yellow; N.L. gen. n. marisflavi of the Yellow Sea).
Cells are straight rods, 0·8–1·1x2·0–3·5 µm on MA. Non-spore-forming. Motile by means of a single polar flagellum. Colonies are smooth, glistening, circular, flat to slightly raised, light brown in colour and 2·0–4·0 mm in diameter after 3 days incubation at 30 °C on MA. Growth occurs at 4 and 42 °C, but not above 43 °C. Growth is observed at pH 5·0, but not at pH 4·5. Optimal growth occurs in the presence of 2–3 % NaCl. No growth occurs in the presence of more than 9 % NaCl. Growth occurs under anaerobic conditions on MA. Casein, tyrosine and Tween 80 are hydrolysed. Aesculin, hypoxanthine, urea, xanthine and xylan (birch wool) are not hydrolysed. When assayed with the API ZYM system, alkaline phosphatase, esterase (C4), esterase lipase (C8), 
-chymotrypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase and N-acetyl-
-glucosaminidase are present and leucine arylamidase is weakly present, but lipase (C14), valine arylamidase, cystine arylamidase, trypsin, -galactosidase, -galactosidase, -glucuronidase, -glucosidase, -glucosidase, -mannosidase and -fucosidase are absent. Acid is produced from D-cellobiose, D-glucose, maltose and D-ribose. Acid is not produced from L-arabinose, D-fructose, D-galactose, lactose, D-mannose, D-melezitose, melibiose, D-raffinose, L-rhamnose, stachyose, sucrose, D-trehalose, D-xylose, adonitol, D-mannitol, myo-inositol or D-sorbitol. Both menaquinones and ubiquinones are present; the predominant menaquinone is MK-7 and the predominant ubiquinones are Q-7 and Q-8. The major fatty acid is iso-C15 : 0. The DNA G+C content is 51 mol% (determined by HPLC). Other phenotypic characteristics are given in Table 1.
The type strain (SW-117T=KCCM 41822T=JCM 12192T) was isolated from sea water of the Yellow Sea in Korea.
Description of Shewanella aquimarina sp. nov.
Shewanella aquimarina (a.qui.ma.ri'na. L. n. aqua water; L. adj. marinus of the sea; N.L. fem. adj. aquimarina pertaining to sea water).
Cells are straight rods, 0·6–0·9x2·0–4·0 µm on MA. Non-spore-forming. Motile by means of a single polar flagellum. Colonies are smooth, glistening, circular, flat to slightly raised, light brown in colour and 2·0–4·0 mm in diameter after 3 days incubation at 30 °C on MA. Growth occurs at 10 and 42 °C, but not at 4 °C or above 43 °C. Growth is observed at pH 5·0, but not at pH 4·5. Optimal growth occurs in the presence of 2–3 % NaCl. No growth occurs in the presence of more than 9 % NaCl. Growth occurs under anaerobic conditions on MA. Casein, tyrosine and Tween 80 are hydrolysed. Aesculin, hypoxanthine, urea, xanthine and xylan (birch wool) are not hydrolysed. When assayed with the API ZYM system, alkaline phosphatase, esterase (C4), esterase lipase (C8), -chymotrypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase and N-acetyl--glucosaminidase are present and leucine arylamidase is weakly present, but lipase (C14), valine arylamidase, cystine arylamidase, trypsin, -galactosidase, -galactosidase, -glucuronidase, -glucosidase, -glucosidase, -mannosidase and -fucosidase are absent. Acid is produced from D-ribose. Acid is not produced from L-arabinose, D-cellobiose, D-fructose, D-galactose, D-glucose, lactose, maltose, D-mannose, D-melezitose, melibiose, D-raffinose, L-rhamnose, stachyose, sucrose, D-trehalose, D-xylose, adonitol, D-mannitol, myo-inositol or D-sorbitol. Both menaquinones and ubiquinones are present; the predominant menaquinone is MK-7 and the predominant ubiquinones are Q-7 and Q-8. The major fatty acid is iso-C15 : 0. The DNA G+C content is 54 mol% (determined by HPLC). Other phenotypic characteristics are given in Table 1.
The type strain (SW-120T=KCCM 41821T=JCM 12193T) was isolated from sea water of the Yellow Sea in Korea.
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ACKNOWLEDGEMENTS |
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