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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, Victoria 3122, Australia
3 Institute of Marine Biology of the Far-Eastern Branch of the Russian Academy of Sciences, 690038, Palchevskogo Str. 17, Vladivostok, Russia
4 UMR 6078 CNRS and Université Nice Sophia-Antipolis, Bat. J. Maetz, F06238 Villefranche sur mer cedex, France
Correspondence
Elena P. Ivanova
eivanova{at}swin.edu.au
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ABSTRACT |
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A full phylogenetic tree and a table showing the complete cellular fatty acid composition of Shewanella waksmanii is available as supplementary data in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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comprises a group of Gram-negative, aerobic and facultatively anaerobic ‘Gammaproteobacteria’ frequently isolated from aquatic habitats and also from clinical sources (MacDonell & Colwell, 1985; Gauthier et al., 1995; Venkateswaran et al., 1999). Shewanella species represent one of the most numerically abundant micro-organisms among readily cultivated marine proteobacteria and currently comprise about 20 species whose names have been validly published. During the last decade, members of this genus have been studied extensively due to their important role in co-metabolic bioremediation of halogenated organic pollutants (Petrovskis et al., 1994), destructive souring of crude petroleum (Semple & Westlake, 1987), the dissimilatory reduction of manganese and iron oxides (Myers & Nealson, 1988), and their ability to produce high proportions of polyunsaturated fatty acids (Russel & Nichols, 1999). In this study we report on the characterization of new bacteria of the genus Shewanella isolated from the sipuncula (peanut worm) Phascolosoma japonicum collected in Troitsa Bay in the Gulf of Peter the Great (Sea of Japan). This work was part of a taxonomic investigation of free living and symbiotrophic marine bacteria from the north-western Pacific Ocean. During the course of this work 70 presumptive Shewanella species of three phenotypes were isolated. The majority of the strains had Shewanella japonica-like phenotype, several had Shewanella colwelliana-like phenotype (E. P. Ivanova et al., unpublished). Only two isolates described here had a number of particular phenotypic properties and formed a separate phylogenetic clade amongst other previously described Shewanella species. Analysis of the results obtained has led us propose the name Shewanella waksmanii sp. nov. for the new strains.
Benthic marine worms (three examples) of the phylum Sipuncula, Phascolosoma japonicum, were collected in 1997 from a depth of 3–5 m (salinity, 32 
, temperature, 18 °C) at the Pacific Institute of Bio-organic Chemistry Marine Experimental Station, in Troitsa Bay, the Gulf of Peter the Great (Sea of Japan). The invertebrates were dissected under aseptic conditions. A tissue homogenate (0·1 ml) was plated onto Marine 2216 agar (Difco) or medium B which contained 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, 1·5 % (w/v) Bacto agar (Difco), 50 % (v/v) of natural sea water, and 50 % (v/v) distilled water at pH 7·8. Plates were incubated aerobically at room temperature (approx. 22–25 °C) for 5, 7 or 10 days. The isolation and purification of the bacterial strains was as described previously (Ivanova et al., 1996). Strains were stored at –80 °C in Marine 2216 broth (Difco) supplemented with 20 % (v/v) of glycerol. In total seven presumptive Shewanella strains out of 45 strains of viable bacteria have been recovered from sipunculas tissue homogenates. Five strains had Shewanella colwelliana-like phenotypes and two strains had distinct phenotypic traits and were studied further in detail.
Unless otherwise indicated, the phenotypic characteristics were studied using standard procedures (Baumann et al., 1972; Smibert & Krieg, 1994) as described elsewhere (Ivanova et al., 1996). The tests for utilization of various organic substrates as sole carbon sources at a concentration of 0·1 % (w/v) were performed in 10 ml tubes of liquid BM medium (Baumann et al., 1972). The bacteria were grown with shaking on a rotary shaker at 160 r.p.m. for 72 h at 25 °C. The ability to oxidize organic substrates was investigated using Biolog-GN plates as described previously (Ivanova et al., 1998). The following physiological and biochemical properties were examined: oxidation/fermentation of glucose, denitrification, catalase and oxidase activities, gelatin liquefaction, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, indole and H2S production, the ability to hydrolyse starch, alginate, chitin, elastin, Tween 80 and casein, and the ability to produce lecithinase. The requirement for Na+ ions was studied on medium that contained (w/v) 0·25 % yeast extract, 0·1 % glucose, 0·02 % KH2PO4, 0·005 % MgSO4.7H2O (pH 7·8). Salt tolerance tests were performed on trypticase soy agar (TSA; Difco) with NaCl concentrations of 0·6–20·0 % (w/v). Dissimilatory iron reduction was tested on LM medium [0·02 % (w/v) yeast extract, 0·01 % (w/v) peptone, 0·6 % (w/v) NaCl, 10 mM sodium bicarbonate, 10 mM HEPES] supplemented with carbon substrates as appropriate (5 mM lactate, 5 mM succinate, 5 mM glycerol, 1 mM acetate), 50 mM ferric citrate, 5 mM sodium molybdate and the colour reagent ferrozine [3-(2-pyridyl)-5,6-bis(4-phenylsulfonic acid)-1,2,4 triazine, pH 7·2] in distilled water. Plates were inoculated and incubated anaerobically at room temperature (approx. 7 d) (with positive and negative controls). Colonies displaying cleared zones were scored as positive for iron reduction.
Haemolytic activity of the strains studied was detected on blood agar (TSA, 40 g l-1; sheep blood, 50 ml; water, 950 ml). Haemolytic activity on mouse erythrocytes and cytotoxicity on Ehrlich cells were tested on butanol extracts of the strains as described earlier (Ivanova et al., 2001). Antibacterial activity was performed by the agar diffusion assay, based on the method described by Barry (1980). Cultures (0·1 ml) of indicator test strains were spread on TSA plates in which circular wells (diameter, 10 mm) had been cut. Samples (0·1 ml) of butanol extracts of the isolates were added to the wells and areas of inhibited bacterial growth were measured after incubation for 48 h at 28 °C. Zones of inhibited growth of the indicator strains surrounding the wells were observed. Mean diameters were measured, and 10 mm subtracted (representing the diameter of the well). Antibacterial activities were tested against Staphylococcus aureus CIP 103594T, Escherichia coli ATCC 15034, Proteus vulgaris NBRC (formerly IFO) 3851T, Enterococcus faecium CIP 104105, Bacillus subtilis ATCC 6051T and the yeast Candida albicans KMM 455. Analysis of fatty acid methyl ethers was performed by GLC as described by Svetashev et al. (1995).
The DNA was extracted from cells grown overnight on B medium following the method of Marmur (1961). The mol% G+C content of the DNA was determined by HPLC (Tamaoka, Komagata, 1984). Levels of genetic relatedness were determined by the fluorometric microdilution plate method (Ezaki et al., 1988; Sawabe et al., 1998). The 16S rRNA gene was amplified and sequenced by MIDI Labs (Newark, USA). Briefly, primers used for the amplification corresponded to Escherichia coli positions 5 and 1540. Amplification products were purified using Microcon 100 (Millipore) molecular mass cut-off membranes and checked for quality and quantity on an agarose gel. Cycle sequencing of the 16S rRNA gene amplification products was carried out using AmpliTaq ES DNA polymerase and Rhodamine dye terminators. The samples were electrophoresed on an ABI Prism 377 DNA Sequencer.
The new 16S rDNA sequence was automatically and then manually aligned by reference to a database of 35 000 already aligned bacterial 16S rRNA gene sequences. Phylogenetic trees were constructed according to three different methods (BioNJ, maximum-likelihood and maximum-parsimony). The BioNJ program from Gascuel (1997), maximum-likelihood and maximum-parsimony programs were from PHYLIP (Phylogeny Inference Package, version 3.573c, distributed by J. Felsenstein, Department of Genetics, UW, Seattle, WA, USA). For the NJ analysis, a matrix distance was calculated according to the Kimura two-parameter correction. Bootstraps were done using 500 replications, BioNJ and Kimura two-parameter corrections. The phylogenetic trees were drawn using NJPLOT (Perrière & Gouy, 1996) and ClarisDraw software for Apple Macintosh. Domains used to construct phylogenetic trees were regions of the small-subunit rDNA sequences available for all sequences and excluding positions likely to show homoplasy.
Strains KMM 3823T and 3836 formed circular, smooth and convex colonies with an entire edge, slightly brown to greenish, 3–5 mm in diameter after 2 days incubation at room temperature (approx. 22–24 °C). Cells of both strains were rod-shaped, 1–2 µm in length and 0·6–0·8 µm in diameter, polarly flagellated and Gram-negative. They did not form endospores. They were phenotypically similar to Shewanella species. Both strains were able to grow anaerobically by fermentation of glucose, a feature observed in some other species of Shewanella: Shewanella frigidimarina, Shewanella gelidimarina, Shewanella hanedai and Shewanella benthica, but the new bacteria did not reduce ferric compounds. Strains KMM 3823T and 3836 did not require organic growth factors. They had an absolute requirement in Na+ ions and grew well at 1–6 % NaCl; no growth was detected at 8 % NaCl. The temperature range was 4–30 °C (optimum at 20–25 °C); no growth was detected at 35 °C. The pH values for growth were 6·0–10·0 (optimum pH 7·5). Both strains were oxidase-, catalase-, haemolysis-positive, but had no cytotoxic or antibacterial activities. Both strains were susceptible to ampicillin and carbenicillin. Strain KMM 3836 indicated susceptibility to gentamicin and kanamycin as well. The novel Shewanella isolates were positive for elastase, gelatinase and DNAase, but negative for amylase, agarase, alginase, laminaranase, chitinase and were able to utilize a wide range of the following carbohydrates (according to Biolog): 
-D-glucose, Tween 40, Tween 80, N-acetyl-D-glucosamine, adonitol, D-arabitol, i-erythritol, D-mannitol, L-rhamnose, D-trehalose, xylitol, methylpyruvate, acetic acid, cis-aconitic acid, citric acid, formic acid, D-gluconic acid, 
-hydroxybutyric acid, p-hydroxyphenylacetic acid, -ketoglutaric acid, DL-lactic acid, propionic acid, quinic acid, sebacic acid, D-mannose, succinic acid, glycyl-L-glutamic acid, D-alanine, L-alanine, laninamide, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, L-histidine, hydroxy L-proline, L-ornithine, L-proline, L-serine, L-pyroglutamic acid, DL-carnitine, urocanic acid, inosine, uridine, L-glutamic acid, L-ornithine, glycerol, DL--glycerol phosphate. Dextrin, m-inositol, L-leucine and uridine were weakly utilized. Phenotypic analysis showed that both isolates were essentially identical to each other and differed only in the susceptibility to gentamicin and kanamycin.
The G+C content of the DNA was 43·0±0·4 mol% for strain KMM 3823T and 42·9±0·4 mol% for strain KMM 3836. DNA–DNA hybridization data revealed a high level of DNA relatedness between KMM 3823T and KMM 3836 (up to 93 %). On the other hand DNA from the KMM 3523T showed rather low relatedness (16–9 %) with the DNAs of the two phylogenetically closest strains Shewanella fidelis KMM 3582T and Shewanella colwelliana ATCC 39565T. These data clearly indicated that the new strains belong to the same genospecies which constitutes a separate species (Wayne et al., 1987; Stackebrandt & Goebel, 1994).
The cellular fatty acids ranged from C12 to C18 and included saturated, monoenoic monounsaturated, straight-chain and iso-branched components (Table 2). In both strains 13 : 0-i, 15 : 0-i, 15 : 0, 16 : 0, 16 : 1(n-7), 17 : 1(n-8) and 20 : 5(n-3) were major components. The level of branched fatty acids was up to 50 % of the total fatty acids for KMM 3823T. Notably, eicosapentaenoic fatty acid, 20 : 5(n-3) (up to 6·7 %) and a high proportion of 15 : 0-i were produced during growth at 28 °C. In their main features, the fatty acid profiles were similar to those reported for Shewanella species (Moule & Wilkinson, 1987; Russel & Nichols, 1999). In spite of the variability of the fatty acid composition between Shewanella species, the specific features of this genus are retained.
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). 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 NJ or MP analysis (Berry & Gascuel 1996). There is no distance bar in Fig. 1 since it would be meaningless because (i) distances are corrected (see above) and (ii) this is a bootstrap tree. Finally the tree shown is rooted as it is a subset of the tree obtained by extracting the first robust clade up from the Shewanella waksmanii leaf. Shewanella waksmanii clustered with Shewanella colwelliana only in the NJ analysis. In parsimony and maximum-likelihood analyses, it had no sister taxon.
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-2). In conclusion, genetic and phylogenetic analyses of 16S rRNA gene sequences are consistent with phenotypic characteristics to suggest that the two strains represent a new species of Shewanella.
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Cells are rod-shaped, 1–2 µm in length and 0·6–0·8 µm in diameter, polarly flagellated and Gram-negative, facultatively anaerobic heterotrophs. Anaerobic growth occurs by fermentation of D-glucose by anaerobic respiration of nitrate. Endospores are not formed. Colonies on Marine 2216 agar are circular, smooth and convex with an entire edge, greenish-brown. Organic growth factors are not required. Growth occurred at 1–6 % of NaCl. Grows at 4–30 °C (optimum 20–25 °C); does not grow at 35 °C. pH range for growth is 6·0–10·0 (optimum pH 7·5). Oxidase and catalase-positive. Haemolytic. Exhibits alginase, elastase and DNase activities. Starch, chitin, agar, alginate and laminaran are not hydrolysed. Susceptible to ampicillin, carbenicillin, gentamicin and kanamycin. D-Glucose utilized as a sole source of carbon. Does not utilize D-galactose, D-fructose, N-acetylglucosamine, succinate, acetate, cellobiose, D-mannose, sucrose, lactose, fumarate, glycerol, 
-aminobutyrate, L-tyrosine. The list of carbon sources oxidized according to Biolog is given in the text. The major cellular fatty acids are i-13 : 0, i-15 : 0, 16 : 0, 16 : 1(n-7) and 20 : 5(n-3).
Based on 16S rRNA gene sequences, belongs to the ‘Gammaproteobacteria’. Isolated from the sipuncula Phascolosoma japonicum in Troitsa Bay in the Gulf of Peter the Great (Sea of Japan). The DNA G+C content is 43·0 mol%. Type strain is KMM 3823T(=CIP 107701T =ATCC BAA-643T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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