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1 Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, 690022 Vladivostok, Prospekt 100 Let Vladivostoku, 159, Russia
2 Institute of Marine Biology, Far-Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia
3 GBF – Gesellschaft für Biotechnologische Forschung GmbH, D-38124 Braunschweig, Germany
4 Institute of Microbiology, Russian Academy of Sciences, 117811 Moscow, Russia
5 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
Correspondence
Erko Stackebrandt
erko{at}dsmz.de
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The GenBank accession number for the 16S rDNA sequence of strain KMM 255T is AJ417594.
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; Humm, 1946; Yaphe & Baxter, 1955; Yaphe, 1957, 1962; Akagawa-Matsushita et al., 1992). The genus Alteromonas, originally described by Baumann et al. (1972) for marine aerobic, Gram-negative, non-fermentative, polarly flagellated bacteria with a DNA G+C content of 37–50 mol%, was later divided into two genera on the basis of phylogenetic analysis: Alteromonas, comprising the single species Alteromonas macleodii, and Pseudoalteromonas, now including 22 species either previously belonging to Alteromonas (Gauthier et al., 1995) or described subsequently (Bozal et al., 1997; Bowman, 1998; Holmström et al., 1998; Ivanova et al., 2000a, 2001; Romanenko et al., 1995; Sawabe et al., 1998, 2000; Venkateswaran & Dohmoto, 2000). The present study was performed to clarify the taxonomic status of four Pseudoalteromonas-like, agarolytic, marine isolates belonging to the genus Pseudoalteromonas.
Four strains were isolated from sea-water samples and ascidian specimens collected from coastal and open oceanic waters during 1985–1992. Sampling, strain isolation and cultivation procedures have been described previously (Romanenko et al., 1994a, b). The strains, designated KMM 255T, KMM 232, KMM 254 and KMM 644, have been deposited in Collection of Marine Micro-organisms (KMM), Pacific Institute of Bioorganic Chemistry, Vladivostok, Russia. The bacteria were maintained on Marine 2216 agar (MA; Difco) plates at 15 °C and stored at -80 °C in 30 % (v/v) glycerol. For reference type strains and their origins, see Table 3. The novel strains were grown routinely at 28 °C on MA or Marine 2216 broth (MB; Difco) and nutrient agar medium, containing natural sea water (SWM). For negative-staining, samples were fixed in 3 % glutaraldehyde/5 % formaldehyde in PBS (100 mM phosphate, 150 mM NaCl, pH 6·9) for 1 h on ice. After being washed in TE buffer (20 mM Tris/HCl, 1 mM EDTA, pH 7·0), samples were adsorbed onto a thin carbon film, washed in TE buffer and negatively stained with 4 % uranyl acetate. After air-drying, samples were examined in a Zeiss EM910 transmission electron microscope at an acceleration voltage of 80 kV. Standard phenotypic characterization of the strains was performed using the methods described by Baumann et al. (1984), Gauthier & Breittmayer (1992) and Smibert & Krieg (1994). Hydrolysis of 
-carrageenan was determined as described by Yaphe & Baxter (1955). Growth at different temperatures (4–40 °C) and pH values (5·0–10·0) was tested by using MB. The sodium-ion requirement and tolerance of NaCl were determined in SWM medium, prepared on the artificial sea-water base supplemented with the appropriate amount of NaCl, ranging from 0 to 15 % (w/v). Acid production from sugars (with 1 %, w/v, of the test sugar) was determined using the method of Leifson (1963). Additional biochemical tests were carried out using API 20NE test kits (bioMérieux) as described by the manufacturer, with the exception that strains were suspended in 3 % (w/v) NaCl solution. Isolates were characterized physiologically by the Biolog GN MicroPlate method. The strains were grown for 24 h at 28 °C on MA 2216 medium and the microtitre plates were inoculated with cells suspended in 2·5 % (w/v) NaCl. Results were read automatically with a spectrophotometer after 24 and 48 h incubation at 28 °C. Antibiotic sensitivity was tested on MA plates by using the agar diffusion method involving discs impregnated with the following antibiotics (content per disc): ampicillin, 10 µg; benzylpenicillin, 10 U; gentamicin, 10 µg; kanamycin, 30 µg; carbenicillin, 25 µg; lincomycin, 15 µg; oleandomycin, 15 µg; polymyxin, 300 U; streptomycin, 30 µg; tetracycline, 30 µg; neomycin, 15 µg; oxacillin, 20 µg; and O/129, 150 µg. Cell morphology and motility were examined by transmission electron and phase-contrast microscopy on bacterial cells grown for 24 h in MB. Analysis of methylated fatty acids and lipids was performed as described by Svetashev et al. (1995) and Ivanova et al. (2000b). Isolation of DNA and determination of the base composition were performed according to Marmur (1961), Marmur & Doty (1962) and Owen et al. (1969). DNA–DNA relatedness was measured spectrophotometrically (De Ley et al., 1970) under optimal reassociation conditions in 2x times; SSC at 64 °C. 16S rRNA gene sequences were determined and compared as described by Rainey et al. (1996). Previously published 16S rRNA gene sequences were obtained from the EMBL/GenBank databases. The analysis of sequences used to generate the dendrogram in Fig. 2 was based on 1391 bases, containing 826 polymorphic sites. Accession numbers are indicated on the dendrogram.
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). The strains required Na+ ions for growth and grew in 1–9 % NaCl. They did not grow at 4–5 or 40 °C; they grew slowly at 6–7 °C and had a temperature optimum ranging between 25 and 28 °C. On MA medium, the bacteria formed whitish or yellowish S- and R-colonies, depressed into the agar. The phenotypic characteristics of the isolates and the phylogenetically closest relatives are summarized in Table 1. The novel isolates were characterized by the hydrolysis of agar, alginate, carrageenan and other polymeric molecules and by the inability to produce acid from D-glucose according to Leifson's method. Weak D-glucose utilization was observed in the API 20NE test. The strains utilized a small number of substrates and did not oxidize D-glucose or other carbohydrates, carboxylic acids, amino acids or other compounds when tested with the Biolog identification system. Table 1 includes the differentiating phenotypic properties of those type strains with which strain KMM255T shares the closest phylogenetic relationships. Comparison with type strains of other non-pigmented, phylogenetically less closely related species, i.e. Pseudoalteromonas antarctica CECT 4664T, Pseudoalteromonas haloplanktis IAM 12915T, Pseudoalteromonas nigrifaciens IAM 13010T, Pseudoalteromonas prydzensis ACAM 620T, Pseudoalteromonas tetraodonis IAM 14160T and Pseudoalteromonas undina NCIMB 2128T (Ivanova et al., 2002), clearly indicated significant phenotypic differences in the formation of melanin-like pigments, the production of hydrolytic enzymes and the utilization of sugars and acids (not shown).
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). The predominant fatty acids were 16 : 0 (20·9–30·4 %) and 16 : 1
7c (38·9–44·0 %). The main phospholipids were phosphatidylethanolamine and phosphatidylglycerol (respectively 66–73 and 23–30 %); these results are in accordance with those found for other Pseudoalteromonas species (Svetashev et al., 1995; Bozal et al., 1997; Ivanova et al., 2000b). Diphosphatidylglycerol (0·9–1·3 %) and bis-phosphatidic acid (2·0–2·7 %) were minor components. It has been noted previously that, except in the case of P. nigrifaciens (1·4 %), diphosphatidylglycerol is not detected in Pseudoalteromonas type strains (Frolova et al., 2000).
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). Comparison of the almost complete 16S rDNA sequence of strain KMM 255T with the corresponding sequences of type strains of Pseudoalteromonas species revealed 99·9 % sequence similarity to Pseudoalteromonas distincta, Pseudoalteromonas elyakovii, Pseudoalteromonas atlantica and Pseudoalteromonas espejiana. Slightly lower values (98·5–99·8 %) were found with the other species indicated in Fig. 2, including the recently described species Pseudoalteromonas issachenkonii (99·6 % similarity) (Ivanova et al., 2002). DNA–DNA similarities determined for strain KMM 255T and a range of closely and more distantly related type strains of species of Pseudoalteromonas were significantly below 60 % (19–45 %), indicating that the four isolates belong to a separate genospecies (Wayne et al., 1987; Stackebrandt & Goebel, 1994). The type strains of P. prydzensis and P. antarctica were not included in the DNA binding studies because the 16S rRNA gene sequence similarities were distinctly lower (respectively 97·2 and 98·5 % similarity) than the gene sequence similarities determined for the other non-pigmented Pseudoalteromonas species. P. issachenkonii was not included because of its recent description. However, as DNA–DNA similarities determined for the type strain KMM 3549T and the type strains of non-pigmented species, including strains that are highly related to the novel genospecies in terms of 16S rRNA gene sequence similarity, were well below 54 %, we are confident that the type strains of the novel genospecies and P. issachenkonii are not members of the same species. Morphological, phenotypic and genomic characteristics suggested that the novel isolates should be assigned to a novel species of Pseudoalteromonas. The moderate DNA–DNA similarities (Table 3) between species correlated with the presence of a combination of distinct metabolic differences determined for the phylogenetically closest relatives (Table 1).
Description of Pseudoalteromonas agarivorans sp. nov.
Pseudoalteromonas agarivorans (a.gar.i.vor'ans. N.L. n. agarum agar-agar, algal polysaccharide; L. v. vorare to devour, to digest; N.L. adj. agarivorans agar-devouring).
Gram-negative, strictly aerobic, rod-shaped cells, 0·8–0·9 µm in diameter and 2·5–3·8 µm long, motile by a single, polar, unsheathed flagellum. Cells with two to four polar flagella are observed. Does not form endospores. Oxidase- and catalase-positive. Sodium ions are essential for growth. Mesophilic and neutrophilic chemo-organotroph. Grows at 7–35 °C, with optimal growth at 20–28 °C; no growth at 4 or 40 °C. Non-pigmented, whitish or pale yellowish S- and R-colonies, depressed into the agar. Positive for lipase, caseinase, DNase, gelatinase and 
-galactosidase. Some strains produce acid from sucrose, maltose and melibiose. ONPG test is positive. As determined by using the Biolog identification system, Tweens 80 and 40, cyclodextran, dextran and glycogen are utilized; acetic and succinic acids are weakly utilized. In addition to metabolic properties used in the differentiation of the species from other Pseudoalteromonas strains indicated in Table 1, negative for the utilization of L-arabinose and gluconate (according to API 20NE), negative for urease, indole production and aesculin hydrolysis and shows no acid formation from L-arabinose, lactose, D-mannose, D-galactose, D-xylose, rhamnose or glycerol. D-Glucose utilization is weak or slow in the API test and negative in the Biolog GN identification system. As determined by the Biolog GN panel, does not utilize cellobiose, L-fucose, D-galactose, D-lactose, D-melibiose, D-raffinose, L-rhamnose, gluconate, m-inositol, erythritol, adonitol, methylpyruvate, mono-methylsuccinate, -hydroxybutyric acid, acetic acid, cis-aconitic acid, citric acid, formic acid, L-lactic acid, propionic acid, succinic acid, bromosuccinic acid, L-aspartic acid, L-glutamic acid, L-serine, L-alanine, L-proline, L-threonine, D-glucuronic acid, 
-ketoglutaric acid, -ketovaleric acid, malonic acid, L-alanylglycine, L-asparagine, hydroxy-L-proline, acetate, DL-lactate, L-leucine, L-histidine, L-ornithine, L-phenylalanine, D-serine, DL-carnitine, 
-aminobutyric acid, uridine, thymidine, putrescine, glucose 1-phosphate or glucose 6-phosphate. Resistant to lincomycin (15 µg), benzylpenicillin (10 U), oxacillin (20 µg), tetracycline (30 µg) and O/129 (150 µg). Major fatty acids are hexadecanoic acid (16 : 0) and hexadecenoic acid (16 : 17c). Dominant phospholipids are phosphatidylethanolamine and phosphatidylglycerol; bis-phosphatidic acid and diphosphatidylglycerol are minor components. DNA G+C content is 42·2–43·8 mol% (thermal denaturation). The strains were isolated from sea water deep in the Pacific Ocean and from the marine ascidians Halocynthia aurantium, Polysyncraton sp. and Clarelina molucensis. The type strain is strain KMM 255T (=DSM 14585T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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