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1 Pacific Institute of Bioorganic Chemistry of the Far-Eastern Branch of the Russian Academy of Sciences, 690022 Vladivostok, Pr. 100 Let Vladivostoku 159, Russia
2 Industrial Research Institute, Swinburne University of Technology, PO Box 218, Hawthorn, Vic 3122, Australia
3 Laboratory of Microbiology, Graduate School of Fisheries Sciences, Faculty of Fisheries, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan
4 Institute of Marine Biology of the Far-Eastern Branch of the Russian Academy of Sciences, 690041 Vladivostok, Russia
5 Muscle Research Unit, Institute for Biomedical Research, The University of Sydney, Sydney 2006, Australia
6 UMR 6543 CNRS and Université de Nice Sophia Antipolis, Centre de Biochimie, Parc Valrose, F-06108 Nice cedex 2, France
Correspondence
Elena P. Ivanova
eivanova{at}swin.edu.au
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ABSTRACT |
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7, amounting to up to 80 % of the total fatty acids. The other characteristic feature was the presence of 18 : 2 isomers. The DNA G+C contents of KMM 3584T and KMM 3554T were respectively 60·0 and 63·7 mol%. The level of DNA similarity between the two strains was 33 %. DNA from KMM 3584T and KMM 3554T had hybridization values of 5–24 % and 10–41 %, respectively, with DNA from the type strains of Sulfitobacter pontiacus, Sulfitobacter brevis, Sulfitobacter mediterraneus and Staleya guttiformis. It is proposed that strains KMM 3584T (=LMG 20554T=ATCC BAA-321T) and KMM 3554T (=LMG 20555T=ATCC BAA-320T) represent two novel species, Sulfitobacter delicatus sp. nov. and Sulfitobacter dubius sp. nov., respectively.
Published online ahead of print on 18 September 2003 as DOI 10.1099/ijs.0.02654-0.
The GenBank accession numbers for the 16S rRNA gene sequences of KMM 3584T and KMM 3554T are AY180103 and AY180102.
Electron micrographs of negatively stained cells of KMM 3554T, a similarity matrix table and an extended phylogenetic tree are available as supplementary material in IJSEM Online.
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). Bacteria of this genus were subsequently detected in samples of natural sea water collected in the Mediterranean Sea (Pukall et al., 1999) and in the hypersaline Ekho Lake of east Antarctica (Labrenz et al., 2000). Phylogenetically, bacteria of this taxon are closely related to bacteria of the recently proposed genus Staleya, which currently contains one species (Staleya guttiformis; Labrenz et al., 2000), and moderately related to bacteria of the genus Roseobacter. According to recent data, representatives of Sulfitobacter can be considered as rather ubiquitous marine bacteria that are widely distributed in coastal and open-ocean environments, namely the Black Sea (Sorokin, 1995), Sargasso Sea (Suzuki et al., 1997) and Antarctica (Labrenz et al., 2000), where they may play an important role in organic sulfur cycling in the ocean.
This study extends our previous investigations into the biodiversity of marine proteobacteria from the Sea of Japan, the north-west Pacific Ocean and other geographical locations (Ivanova et al., 1996, 1998, 2000; Sawabe et al., 2000). During isolation studies, bacteria of various taxonomic groups, including species of Shewanella, Marinobacter, Halomonas and Pseudoalteromonas, have been isolated (E. P. Ivanova, unpublished results; Kurilenko et al., 2001). However, only two strains with Sulfitobacter-like phenotypes have been tentatively identified. The strains examined in this study were isolated from a starfish (Stellaster equestris) and sea grass (Zostera marina). The starfish was collected in October 1998 at a depth of 100 m (salinity 30 
, temperature 15 °C) in the South China Sea (26° 28·3' N 122° 29·0' E). The sea grass was collected in July 1998 at a depth of 5–8 m (salinity 33 , temperature 12 °C) at the Pacific Institute of Bio-organic Chemistry Marine Experimental Station, Troitza Bay, Gulf of Peter the Great, Sea of Japan. The starfish and sea grass were pre-rinsed in sterilized sea water and pieces of tissue (about 3 g) were aseptically removed. Strains were isolated by plating samples of tissue homogenate (0·1 ml) onto marine agar 2216 (Difco) plates and medium B plates. Medium B contained the following [in 50 % (v/v) natural sea water and 50 % (v/v) distilled water at pH 7·5–7·8, as described previously (Ivanova et al., 1996)]: 0·2 % (w/v) Bacto peptone (Difco); 0·2 % (w/v) casein hydrolysate (Merck); 0·2 % (w/v) Bacto yeast extract (Difco); 0·1 % (w/v) glucose; 0·02 % (w/v) KH2PO4; 0·005 % (w/v) MgSO4.7H2O; and 1·5 % (w/v) Bacto agar (Difco).
Phenotypic properties used for characterization of Sulfitobacter species were assessed using standard procedures (Smibert & Krieg, 1994) and as described elsewhere (Ivanova et al., 1996, 1998). The bacteria were grown at 22–24 °C. Motility was studied in hanging drop preparations. The following physiological and biochemical properties were examined: oxidation/fermentation of glucose (Hugh & Leifson, 1953); Gram staining; reduction of nitrate and nitrite; catalase (with 5 % H2O2) and oxidase (Kóvacs, 1956) activities; gelatin liquefaction; production of arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, poly-
-hydroxybutyrate and acetoin (Voges–Proskauer test); sodium requirement [0, 1, 3, 6, 8, 10, 12, 15 % (w/v) NaCl]; indole and H2S production; and the ability to hydrolyse starch, Tween 80, casein, DNA, chitin, agar and alginate. The temperature range for growth was examined on marine agar incubated at 4, 10, 30, 35, 37 and 42 °C. Haemolytic activity of the strains was detected on blood agar containing 40 g trypticase soy agar in 50 ml sheep blood and 950 ml water. Oxidative utilization of 95 carbon sources was tested using Biolog GN Microplates (Rüger & Krambeck, 1994) as described elsewhere (Ivanova et al., 1998). The ability to oxidize sulfite was tested as described by Pukall et al. (1999). Susceptibility to antibiotics was tested by the conventional diffusion plate technique using solid medium B and discs impregnated with following antibiotics: kanamycin (30 µg), ampicillin (10 µg), benzylpenicillin (10 U), streptomycin (10 µg), erythromycin (15 µg), gentamicin (10 µg), oxacillin (20 U), lincomycin (15 µg), carbenicillin (100 U), vancomycin (30 µg), tetracycline (30 µg), oleandomycin (15 µg) and O/129 (150 µg).
Cellular morphology was examined by phase-contrast light microscopy of 24-h-old cultures grown on agar plates. Electron micrographs of negatively stained cells were prepared using a Zeiss EM 10 CA electron microscope (80 kV). A drop of particle-free (autoclaved and ultracentrifuged) distilled water was placed on the culture. The sample (30 µl) of resulting bacterial suspension was applied to carbon- and Formvar-coated 400-mesh copper grids, a drop of 1·25 % uranyl acetate was added and the bacteria were allowed to adhere for 1 min at room temperature. Superfluous liquid was gently removed using a piece of filter paper.
Lipids were extracted from wet cells by the method of Bligh & Dyer (1959). Two-dimensional micro-TLC of polar lipids was carried out according to the method of Svetashev & Vaskovsky (1972) using chloroform/methanol/benzene/28 % NH4OH (65 : 30 : 10 : 6, by vol.) for the first direction and chloroform/methanol/benzene/acetone/acetic acid/water (70 : 30 : 10 : 5 : 4 : 1, by vol.) for the second one. Non-specific detection of lipids on the TLC was performed with a 10 % H2SO4 solution in methanol with charring at 180 °C (Kates, 1986). The following specific reagents were used: for phospholipids, see Vaskovsky et al. (1975); 2 % ninhydrin in acetone for amino-containing lipids; Dragendorff's reagent for choline lipids; and anthrone spray (0·5 % anthrone in benzene and 5 % H2SO4 in water) for glycolipids. Phosphorus analysis was carried out according to Vaskovsky et al. (1975). The phospholipid compositions of the isolates studied were generally similar. Phosphatidylglycerol was the major constituent of the phospholipids, accounting for 66 % total phospholipid. The strains contained significant amounts of phosphatidylethanolamine (up to 14·2 %) and phosphatidylcholine (up to 18 %). Diphosphatidylglycerol was present in smaller amounts (3–8 %).
Fatty acid methyl esters were prepared as described elsewhere (Svetashev et al., 1995) and analysed on a Shimadzu GC-14A GC with an FID using both a non-polar SPB-5 fused-silica column (30 mx0·25 mm i.d.) at 210 °C and a polar Supelcowax-10 fused-silica column (30 mx0·25 mm i.d.) at 200 °C. Analysis of cellular fatty acids of Sulfitobacter-like isolates revealed that the strains studied had a characteristic genus-specific pattern of fatty acids. Of 17 identified fatty acids, cis-vaccenic acid (18 : 17) was the major component (up to 80 % total fatty acids) and 16 : 0 and 18 : 19 were detected at levels of 4·4–7·8 %. 10 : 0 3-OH, 16 : 17, 17 : 0 and 18 : 2 isomers were present as minor components, which is consistent with the data of Pukall et al. (1999) and Labrenz et al. (2000).
Sulfitobacter pontiacus DSM 10014T, Sulfitobacter mediterraneus ATCC 700856T and Sulfitobacter brevis ATCC BAA-4T, obtained from the German Collection of Microorganisms and the American Type Culture Collection, were used for comparing phenotypic properties and DNA–DNA hybridization experiments. Staleya guttiformis DSM 11458T was a generous gift from P. Hirsch (Institut für Allgemeine Mikrobiologie, Kiel, Germany). All the reference strains were routinely cultured on marine agar 2216 plates (Difco) and PYGV agar plates (Staley, 1968). DNA was isolated from the strains by the method of Marmur (1961). The G+C content of the DNA was determined using the thermal denaturation method (Marmur & Doty, 1962). DNA–DNA hybridization experiments were performed using covalent attachment of the DNA in micro-wells according to the method evaluated by Christensen et al. (2000). The level of DNA–DNA relatedness between the two strains studied was 33 % and they were therefore genotypically assigned to separate species. The genetic similarity of KMM 3584T to type strains of the genus Sulfitobacter and Staleya guttiformis was rather low (5–24 %) (Table 1); for KMM 3554T, the similarity was 10–41 %. Based on the generally accepted criterion of the definition of genomic species (Wayne et al., 1987), strains KMM 3584T and KMM 3554T are representatives of novel species.
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, b). The 16S rRNA gene sequences of KMM 3584T and KMM 3554T were aligned automatically and then manually by reference to a database of 86 000 previously aligned bacterial 16S rRNA gene sequences. Phylogenetic trees were constructed according to three methods [BIONJ, maximum-likelihood (ML) and maximum-parsimony (MP)]. For neighbour-joining (NJ) analysis, distance matrices were calculated using the Kimura two-parameter correction. BIONJ was according to Gascuel (1997) and ML and MP were from PHYLIP (Phylogeny Inference Package, version 3.573c, distributed by J. Felsenstein, Department of Genetics, UW, Seattle, WA, USA). Only parts of the sequences that could be properly aligned were used for the tree depicted; they correspond to positions 60–1273 of the KMM 3554T sequence. The phylogenetic trees were drawn using NJPLOT (Perrière & Gouy, 1996). Fig. 1 shows a consensus tree between NJ (bootstrap analysis, 1000 replications), ML and MP analysis. The topology shown is that of the bootstrap tree, as it has been demonstrated that this topology is often better than that of a simple tree (Berry & Gascuel, 1996).
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97·8 %) (but see the table available as supplementary material in IJSEM Online). An initial first analysis included the 79 most similar sequences as retrieved by BLAST on EMBL and EMBL new (a tree is available as supplementary material in IJSEM Online). Removal of sequences pertaining to species that were uncultured and not validly named led to a dataset of 14 sequences that were visually aligned and analysed by all three methods (see Fig. 1
). The two KMM sequences grouped robustly with ‘O. indoliflex’, a species that is yet to be described, but not with any species with validly published names, suggesting that each of these sequences represents a novel bacterial species, as confirmed by DNA–DNA hybridization experiments (Table 1). These two species clustered with the type species of the genus Sulfitobacter (Sulfitobacter pontiacus) according to NJ and ML, but not MP, and the degree of bootstrap replication was low (39 %), suggesting that the genus Sulfitobacter might be subject to revision in the future, probably to include only the type species of the genus. Such a revision may require phylogenetic analyses of more housekeeping genes; it is therefore suggested that the two novel species be assigned to the genus Sulfitobacter for the time being.
The two novel species can be distinguished from other Sulfitobacter species and Staleya guttiformis by a number of phenotypic traits (Table 2). For example, strain KMM 3584T is able to hydrolyse gelatin and alginate and does not utilize melibiose, whereas strain KMM 3554T is more halophilic, hydrolyses only gelatin and utilizes citrate and melibiose. Both novel species are unable to produce DNase or lipase. The names Sulfitobacter delicatus sp. nov. and Sulfitobacter dubius sp. nov. are proposed for KMM 3584T and KMM 3554T, respectively.
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Rod-shaped cells, single, about 0·7–0·9 µm in diameter. Gram-negative. Non-motile. Chemo-organotroph with respiratory metabolism. Colonies are uniformly round, 1–3 mm in diameter, regular, convex, smooth and slightly yellowish after incubation for 48–74 h on marine agar. No diffusible pigment is produced in the medium. Does not form endospores. Accumulates poly--hydroxybutyrate as an intracellular reserve product. Oxidase- and catalase-positive. Requires Na+ or sea water for growth. Growth occurs in media containing 1–8 % NaCl. Mesophilic. Grows at 12–37 °C and pH 6·0–10·0; optimum growth is observed at 25 °C and pH 7·5–8·0. No growth is detected at 40 °C. Decomposes gelatin and alginate. Agar, starch, casein, laminarin, Tween 80 and DNA are not hydrolysed. From the 95 carbon sources tested, according to Biolog, 
-cyclodextrin, glycogen, i-erythritol, psicose, D-raffinose, L-rhamnose, acetic acid, D-galactonic acid lactone, D-galacturonic acid, D-glucuronic acid, -ketovaleric acid, glucuronamide, L-leucine, L-ornithine, D-serine, DL-carnitine, urocanic acid, thymidine, phenylethylamine, putrescine, 2-aminoethanol, 2,3-butandiol, DL--glycerolphosphate and glucose 1-phosphate are not utilized and L-fucose, D-galactose, gentiobiose, -lactose, D-mannitol and hydroxyproline are only weakly utilized. Susceptible to ampicillin, benzylpenicillin, gentamicin, kanamycin, carbenicillin, neomycin, oleandomycin and streptomycin; not susceptible to polymyxin or tetracycline. Phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine are the major phospholipids. The main cellular fatty acid is cis-vaccenic acid (approx. 80 %).
The type strain is KMM 3584T (=LMG 20554T=ATCC BAA-321T). The G+C content of the DNA of the type strain is 60·3 mol%. Isolated from a starfish (Stellaster equestris) collected from the South China Sea.
Description of Sulfitobacter dubius sp. nov.
Sulfitobacter dubius (du'bi.us. L. masc. adj. dubius doubtful).
Rod-shaped cells, single, about 0·6–0·8 µm in diameter and 1·2–1·5 µm long with a single subpolar flagellum (see figure available as supplementary material in IJSEM Online). Gram-negative. Chemo-organotroph with respiratory metabolism. Colonies are uniformly round, 1–3 mm in diameter, regular, convex, smooth, slightly yellowish after incubation for 48 h on marine agar. No diffusible pigment is produced in the medium. Does not form endospores. Accumulates poly--hydroxybutyrate as an intracellular reserve product. Oxidase- and catalase-positive. Requires Na+ or sea water for growth. Growth occurs in media containing 1–12 % NaCl. Grows at 10–30 °C and pH 6·0–11·0; optimum growth is observed at 25 °C and pH 7·5–8·0. No growth is detected at 35 °C. Decomposes gelatin. Agar, starch, casein, laminarin, alginate, Tween 80 and DNA are not hydrolysed. From the 95 carbon sources tested, according to Biolog, i-erythritol, D-raffinose, thymidine, phenylethylamine, putrescine and 2-aminoethanol are not utilized and -cyclodextrin, glycogen, L-fucose, D-galactose, L-rhamnose, D-sorbitol, D-galactonic acid lactone, D-galacturonic acid, glucuronamide, L-phenylalanine, L-pyroglutamic acid, D-serine and glucose 1-phosphate are only weakly utilized. Susceptible to ampicillin, benzylpenicillin, gentamicin, kanamycin, carbenicillin, neomycin, oleandomycin and streptomycin; not susceptible to polymyxin, tetracycline or lincomycin. Phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine are the major phospholipids. The main cellular fatty acid is cis-vaccenic acid (approx. 80 %).
The type strain is KMM 3554T (=LMG 20555T=ATCC BAA-320T). The G+C content of DNA of the type strain is 63·7 mol%. Isolated from sea grass (Zostera marina) collected from the Sea of Japan.
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ACKNOWLEDGEMENTS |
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E. P. Ivanova, N. M. Gorshkova, N. V. Zhukova, A. M. Lysenko, E. A. Zelepuga, N. G. Prokof'eva, V. V. Mikhailov, D. V. Nicolau, and R. Christen Characterization of Pseudoalteromonas distincta-like sea-water isolates and description of Pseudoalteromonas aliena sp. nov. Int J Syst Evol Microbiol, September 1, 2004; 54(5): 1431 - 1437. [Abstract] [Full Text] [PDF]
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