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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 UMR 6078 CNRS and Université Nice Sophia-Antipolis, Bat. J. Maetz, F-06238 Villefranche sur mer cedex, France
Correspondence
Elena P. Ivanova
Ivanova. eivanova{at}swin.edu.au
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ABSTRACT |
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-Proteobacteria within the members of the genus Shewanella. KMM 3582T showed the highest similarity (97·1 and 97·4 %, respectively) to Shewanella pealeana and Shewanella gelidimarina. The G+C contents of the DNAs of the two strains studied were 45·0 mol%. The level of DNA–DNA relatedness between the two strains was 82 %, indicating that they represent a single genospecies. These organisms were slightly pinkish, Gram-negative, polarly flagellated, facultatively anaerobic, mesophilic (with temperature range from 4 to 30 °C), neutrophilic and haemolytic and were able to degrade alginate, gelatin and DNA. The novel organisms were susceptible to gentamicin, lincomycin, oleandomycin, streptomycin and polymyxin. The predominant fatty acids were characteristic for shewanellae: 13 : 0-i, 15 : 0-i, 16 : 0 and 16 : 1
7. Eicosapentaenoic acid, 20 : 53, was not detected. Phylogenetic evidence, together with phenotypic characteristics, showed that the two bacteria constitute a novel species of the genus Shewanella. The name Shewanella fidelis sp. nov. is proposed, with the type strain KMM 3582T (=LMG 20551T =ATCC BAA-318T).
The full list of sequences used in the neighbour-joining analysis is available as supplementary material in IJSEM Online (http://ijs.sgmjournals.org).
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TOPABSTRACTMAIN TEXTREFERENCES |
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-Proteobacteria that are mainly associated with aquatic habitats (MacDonell & Colwell, 1985
; Gauthier et al., 1995; Venkateswaran et al., 1999). During the last decade, the bacteria of this genus have been studied extensively because of their important roles in co-metabolic bioremediation of halogenated organic pollutants (Petrovskis et al., 1994), destructive souring of crude petroleum (Semple & Westlake, 1987) and the dissimilatory reduction of manganese and iron oxides (Myers & Nealson, 1988) and their ability to produce high proportions of polyunsaturated fatty acids (Russell & Nichols, 1999). In this study, we report the characterization of novel bacteria of the genus Shewanella isolated from sediment and sea-water samples from different geographical areas, the South China Sea and the Sea of Japan. This work was part of a taxonomic investigation of free-living and symbiotrophic marine bacteria of the Far-Eastern region and in the course of this work, a number of strains with phenotypes similar to that of the genus Shewanella was isolated. The two isolates described here formed a distinct phylogenetic clade among other previously described shewanellae and constitute a novel species, for which we propose the name Shewanella fidelis sp. nov.
A sediment sample was collected in 1998 from a depth of 73 m in the South China Sea (29° 33·2'N, 125°14·2'E). Sea-water samples were collected in 1997 from a depth of 0·5–1·5 m (salinity 32 
, temperature 15 °C) at the Pacific Institute of Bio-organic Chemistry Marine Experimental Station, Troitza Bay, Gulf of Peter the Great, Sea of Japan. All samples were 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) natural sea water and 50 % (v/v) distilled water at pH 7·0. Plates were incubated aerobically at room temperature (
20–22 °C) for 5–10 days and subsequently purified. The bacterial strains were isolated and purified as described previously (Ivanova et al., 1996). Strains were stored at -80 °C in marine 2216 broth (Difco) supplemented with 20 % (v/v) glycerol.
Unless otherwise indicated, phenotypic characteristics were studied using standard procedures (Baumann et al., 1972; Smibert & Krieg, 1994) as described elsewhere (Ivanova et al., 1996; Sawabe et al., 2000). 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. 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-NaOH, pH 7·2] supplemented with carbon substrates as appropriate (5 mM lactate, succinate or glycerol or 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] in distilled water. Plates were inoculated and incubated anaerobically at room temperature for about 7 days (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 (l-1: trypticase soy agar, 40 g; 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 previously (Ivanova et al., 2001).
Antibacterial activity was assessed by the agar diffusion assay, based on the method described by Barry (1980). Cultures (0·1 ml) of indicator test strains were spread on tryptic soy agar (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 IFO 3851, Enterococcus faecium CIP 104105, Bacillus subtilis ATCC 6051T and the yeast Candida albicans KMM 455.
The analysis of fatty acid methyl ethers was performed by GLC as described previously by Svetashev et al. (1995).
DNA was extracted from cells grown overnight on medium B following the method of Marmur (1961). The 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., 1998b). The type strain of Shewanella gelidimarina was kindly provided by Dr J. Bowman (University of Tasmania, Hobart, Australia) and the type strain of Shewanella pealeana was kindly provided by Dr M. Leonardo (Center for Great Lakes Studies, University of Wisconsin–Milwaukee, USA).
Bacterial DNAs for PCR were prepared using the Promega Wizard genomic DNA extraction kit according to the instruction manual. Aliquots of 100 ng DNA were used in a PCR to amplify the small-subunit rRNA genes as described previously by Sawabe et al. (1998a, b). PCR conditions were as follows: initial denaturation step at 94 °C for 180 s, annealing step at 55 °C for 60 s and an extension step at 72 °C for 90 s. The thermal profile then consisted of 30 cycles. The amplification primers (Sawabe et al., 1998a) used in this study gave a 1·5 kb PCR product and corresponded to positions 25–1521 of the Escherichia coli 16S rDNA sequence. The PCR products were purified using a Promega Wizard PCR Preps DNA purification kit and sequenced directly by using a Taq FS dye terminator sequencing kit (ABI) following the protocol recommended by the manufacturer. DNA sequencing was performed with an Applied Biosystems model 310 automated sequencer. Nine sequencing primers were used for sequencing (Sawabe et al., 1998a).
The new 16S rDNA sequences were automatically and then manually aligned by reference to a database of 35 000 already-aligned bacterial 16S rDNA sequences. Phylogenetic trees were constructed according to three different methods (BioNJ, maximum-likelihood and maximum-parsimony). The BioNJ program from Gascuel (1997) and maximum-likelihood and maximum-parsimony programs from PHYLIP (phylogeny inference package version 3.573c, distributed by J. Felsenstein, Department of Genetics, UW, Seattle, WA, USA) were used. For the neighbour-joining analysis, matrix distances were calculated according to Kimura's two-parameter correction. Bootstraps were done using 500 replications, BioNJ and Kimura's two-parameter correction. 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.
The two heterotrophic marine strains KMM 3582T and KMM 3589, isolated from sediment and sea-water samples collected from the South China Sea and the Sea of Japan, formed circular, smooth and convex colonies with an entire edge that were slightly pinkish and 3–5 mm in diameter after 2–4 days incubation at room temperature (22–24 °C). Cells of both strains were rod-shaped, 1–2 µm long and 0·6–0·8 µm in diameter, polarly flagellated and Gram-negative. They did not form endospores. The bacteria were phenotypically similar to Shewanella species. Both strains were able to grow anaerobically by fermentation of glucose, a feature observed for some other Shewanella species (Shewanella frigidimarina, Shewanella gelidimarina, Shewanella hanedai and Shewanella benthica), but did not reduced ferric compounds. Strains KMM 3582T and KMM 3589 did not require organic growth factors or sodium ions or sea water for growth and grew well in 1–8 % NaCl. No growth was detected at 10 % NaCl. The temperature range for growth was 4–30 °C, with optimum growth at 20–25 °C. No growth was detected at 35 °C. The pH for growth was pH 6·0–10·0, with optimum growth at pH 7·5. Both strains were oxidase-, catalase- and haemolysis-positive but had no cytotoxic or antibacterial activities. Both were susceptible to gentamicin, lincomycin, oleandomycin, streptomycin and polymyxin. The novel Shewanella isolates were positive for alginase, gelatinase and DNase but negative for amylase, agarase, 
-carrageenase, laminarinase, chitinase and elastase and were able to utilize a limited number of carbohydrates. Phenotypic analysis showed that the two isolates were essentially similar and differed only in the ability to hydrolyse Tween 80.
The G+C content of the DNA was 45·0±0·4 mol% for strain KMM 3582T and 44·9±0·4 mol% for strain KMM 3589. DNA–DNA hybridization data revealed a high level of DNA relatedness between KMM 3582T and KMM 3589 (up to 82·4 %), indicative of strains of the same genospecies (Wayne et al., 1987).
The cellular fatty acids ranged from C12 to C18 and included saturated, monoenoic, straight-chain and iso-branched components (Table 1). In both strains, 13 : 0-i, 15 : 0-i, 15 : 0, 16 : 0, 16 : 17 and 17 : 18 were major components. The level of branched fatty acids was up to 34·7 % of the total fatty acids for KMM 3582T and 25·8 % for KMM 3589. Eicosapentaenoic acid, 20 : 53, was not detected in either isolate. In their main features, the fatty acid profiles were similar to those reported for Shewanella species (Moule & Wilkinson, 1987; Russell & Nichols, 1999). In spite of the variability of the fatty acid composition between Shewanella species, the specific features of this genus are maintained.
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-Proteobacteria and more precisely, that they are included in the clade that is formed by species of the genus Shewanella (Fig. 1). The topology of the phylogenetic tree shown is that of the bootstrap analysis, as it has been demonstrated that this topology is often better than that of a simple neighbour-joining analysis (Gascuel, 1997). As a result, there is no distance bar in this tree; note also that one should consider the distance bar with caution in a tree, as the distance bar represents the distances calculated after correction (Kimura's two-parameter; Jukes & Cantor, 1969) and that the lengths of the branches do not represent simply the real number of differences between the sequences themselves. The analysis was done with all 30 sequences, but the figure shown is a subset of the total analysis, restricted to the Shewanella clade. The full list of 30 sequences is available as supplementary material in IJSEM Online (http://ijs.sgmjournals.org). Percentages of 16S DNA similarity to other available sequences were calculated by parsing the result of a BLAST analysis of KMM 3582T on the Bacteria division (15 September 2001) with the options ‘all default’ and ‘no filter’. Strains KMM 3582T and KMM 3589 formed a distinct branch inside the robust cluster that comprised species Shewanella hanedai, Shewanella woodyi, Shewanella gelidimarina, Shewanella colwelliana, Shewanella pealeana, Shewanella benthica and Shewanella violacea. The sequences of strains KMM 3582T and KMM 3589 were 98·9 % similar and respectively showed 97·4 and 97·1 % similarity to and 39 and 43 differences from their nearest phylogenetic relatives, Shewanella gelidimarina and Shewanella pealeana.
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). These data are in agreement with the conclusion that strains KMM 3582T and KMM 3589 belong to a novel species of Shewanella, on the basis that strains with DNA reassociation values of less than 70 % belong to separate species (Wayne et al., 1987). Since other phylogenetically close Shewanella species, Shewanella hanedai, Shewanella woodyi, Shewanella colwelliana, Shewanella benthica and Shewanella violacea, had only 96·1 % or less 16S rDNA sequence similarity, genetic relatedness of less than 60–70 % between these species and the novel isolates is assumed, as has been shown previously for shewanellae by Venkateswaran et al. (1999) and for other taxa by Stackebrandt & Goebel (1994).
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) and Shewanella gelidimarina (Bowman et al., 1997) by the tolerance of 8 % NaCl and the presence of haemolytic activity. The strains can also be differentiated from Shewanella pealeana by the ability to produce gelatinase and the inability to utilize D-galactose, lactate, succinate and citrate and from Shewanella gelidimarina by the inability to produce amylase and chitinase and the utilization of lactate (Table 3).
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Description of Shewanella fidelis sp. nov.
Shewanella fidelis (fi.de'lis. L. fem. adj. fidelis true, referring to a true member of the genus).
The cells are rod-shaped, 1–2 µm long 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. No ferric compounds can serve as electron donors. No endospores are formed. Colonies on marine 2216 agar are circular, smooth and convex with an entire edge, slightly pinkish. Organic growth factors and sodium ions or sea water are not required. Growth also occurs at 1–8 % NaCl. Temperature for growth is 4–30 °C, with optimum growth at 20–25 °C. No growth at 35 °C. The pH range for growth is 6·0–10·0, with optimum growth at pH 7·5. Oxidase- and catalase-positive. Haemolytic. Exhibits alginase, gelatinase and DNase activities. Starch, chitin, elastin, agar, -carrageenan and laminaran are not hydrolysed. Susceptible to gentamicin, lincomycin, oleandomycin, streptomycin and polymyxin. D-Glucose is 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 or L-tyrosine. The major cellular fatty acids are i-15 : 0, 16 : 0 and 16 : 17. The G+C content of the DNA is 45·0 mol%.
The type strain, KMM 3582T (=LMG 20551T =ATCC BAA-318T), was isolated from sediment of the South China Sea. A reference strain, strain KMM 3589, was isolated from sea water of the Sea of Japan.
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ACKNOWLEDGEMENTS |
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