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1 UMR 6539, Centre National de la Recherche Scientifique et Université de Bretagne Occidentale, Technopôle Brest-Iroise, Place Nicolas Copernic, 29280 Plouzané, France
2 Marine Ecosystems Research Department, Japan Marine Science and Technology Centre, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
3 Laboratoire de Microbiologie et de Biotechnologie des Extrêmophiles, Département de Valorisation des Produits, IFREMER, Centre de Brest, BP 70, 29280 Plouzané, France
4 DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Mascheroder Weg 1b, D-38124 Braunschweig, Germany
5 Institute of Microbiology, RAS Prospekt 60 Let Oktyabrya 7/2, 117312 Moscow, Russia
Correspondence
Laurent Toffin
toffin{at}jamstec.go.jp
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7c, 15 : 0 iso, 16 : 0 and 13 : 0 iso. The G+C content of the DNA was 44·9 mol%. On the basis of 16S rRNA gene sequences, strain LT13aT was shown to belong to the 
-Proteobacteria, being closely related to Shewanella putrefaciens (98 %), Shewanella oneidensis (97 %) and Shewanella baltica (96 %). Levels of DNA homology between strain LT13aT and S. putrefaciens, S. oneidensis and S. baltica were <20 %, indicating that strain LT13aT represents a novel species. Genetic evidence and phenotypic characteristics showed that isolate LT13aT constitutes a novel species of the genus Shewanella. Because of the deep origin of the strain, the name Shewanella profunda sp. nov. is proposed, with LT13aT (=DSM 15900T=JCM 12080T) as the type strain.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Shewanella profunda LT13aT is AY445591.
An electron micrograph and details of the growth behaviour and fatty acid and polar lipid compositions of strain LT13aT are available as supplementary material in IJSEM Online.
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). Recently, a novel methanogenic species, Methanoculleus submarinus, was isolated from Nankai Trough sediment (Mikucki et al., 2003). The genus Shewanella comprises Gram-negative, facultative anaerobes that belong to the -Proteobacteria (MacDonell & Colwell, 1985) and is typically one of the deep-sea bacterial genera (DeLong et al., 1997). This genus includes psychrophilic and mesophilic species originating mainly in freshwater and marine habitats (Jensen et al., 1980; Semple & Westlake, 1987; Myers & Nealson, 1988; Brettar & Hölfe, 1993; Nogi et al., 1998; Venkateswaran et al., 1998; Ivanova et al., 2003). Thermophilic Shewanella-like bacteria were recently cultivated (Ghosh et al., 2003). The genus Shewanella was divided into two subgenera on the basis of phylogenetic structure, growth properties in relation to pressure, and polyunsaturated fatty acid production (Kato & Nogi, 2001).
The novel isolate was obtained from a sediment sample that was collected 4·15 m below the seafloor at a water depth of 4790·7 m in the Pacific Ocean at the Nankai Trough offshore from Japan (site 1173: 32° 14·7' N 135° 1·5' E) between 28 and 07 June 2000 on Leg 190 of the Ocean Drilling Program (site 1173). All details of the environmental conditions, sampling and subsampling procedures have been reported previously (Cragg et al., 1992a, b; Parkes et al., 1995; Moore et al., 2001).
Enrichment cultures were conducted anaerobically in medium containing the following (l–1): 30 g sea salts (Sigma), 2 g yeast extract (Difco), 2 g peptone (Difco) and 0·5 mg resazurine. The medium was adjusted to pH 7·0 and autoclaved. Sterile additions were as follows: 10 ml 1 M NaHCO3, 1 g CH3COONa.3H2O, 1 ml trace elements solution (Widdel & Bak, 1992), 1 ml vitamin solution (Widdel & Bak, 1992), 1 ml 0·01 % (w/v) thiamine (Widdel & Bak, 1992), 1 ml 0·005 % (w/v) vitamin B12 (Widdel & Bak, 1992), 1 ml growth factor (Pfennig et al., 1981), 0·3 g KH2PO4, 0·5 mg sodium selenate and 0·5 mg sodium tungstate. The final pH of the medium was about 6·8. Medium was distributed into vials and initial vial preparation involved sequential evacuation and gassing with H2/CO2 (20 : 80, v/v) at 200 kPa. The medium was then reduced by using 0·5 g sodium sulphide l–1. Sediment suspensions were inoculated (10 % final, v/v) into the medium and incubated at 25 °C. Growth of motile, rod-shaped micro-organisms was observed in enrichment cultures after 2 days incubation at 25 °C. Positive cultures were transferred at least three times at 10 % inoculum into fresh medium and spread on plates containing 1 % (w/v) agar (Difco). On agar plates, colonies were circular and transparent; they were 1–2 mm in diameter after 3–5 days incubation at 30 °C. Old cultures were slightly pinkish. One isolate was purified and designated LT13aT (=DSM 15900T=JCM 12080T).
Isolate LT13aT was grown routinely in the following medium (YP) containing the following (l–1): 23 g NaCl, 3 g MgCl2, 0·15 g CaCl2, 0·5 g KCl, 4 g Na2SO4, 1 g yeast extract (Difco), 2 g peptone (Difco), 3·6 g PIPES buffer and 0·25 g KH2PO4. The pH of the medium was adjusted to 7·2 before autoclaving. Unless indicated otherwise, cultures were incubated aerobically at 30 °C and atmospheric pressure. Stock cultures of isolate LT13aT were stored in culture medium at 4 °C. For long-term storage, pure cultures were stored at –80 °C in the same medium containing 20 % (v/v) glycerol.
The isolate was tested for Gram-staining, cell size, morphology [using phase-contrast microscopy (model BH2; Olympus) and electron microscopy (JEM 100 CX II; JEOL) after negative staining with 2 % (w/v) uranyl acetate] and for cytochrome oxidase and catalase (3 % H2O2).
Nankai Trough strain LT13aT appeared as single rods that were approximately 0·5–0·7x2·5–3·5 µm (see Supplementary Fig. A in IJSEM Online) during the exponential phase of growth. Cells were motile by means of a single polar flagellum (see Supplementary Fig. A in IJSEM Online). They did not form endospores and spores were not produced in any phase of growth under any growth conditions tested. Cells stained Gram-negative and were oxidase-positive and catalase-negative.
To determine the optimum temperature, pH and NaCl concentration, cells were grown in YP medium. Growth at the following temperatures was tested: 4, 10, 15, 20, 25, 30, 37 and 40 °C. Growth at the following NaCl concentrations was tested: 0, 5, 10, 15, 20, 30, 40, 50, 60, 70, 80 and 90 g l–1. Growth at the following pH values was tested: 3·0, 4·0, 5·0, 5·5, 6·0, 6·5, 7·0, 7·5, 8·0, 8·5, 9·0 and 10·0, as described by Widdel & Bak (1992). The effect of the following hydrostatic pressures on growth rates of strain LT13aT was determined: 0·1, 10, 20, 30, 40 and 50 MPa at 30 °C, as previously described (Kato et al., 1995).
Utilization of carbohydrates (listed in Table 1) as catabolic substrates was tested aerobically in a modified YP liquid medium from which carbon sources were omitted. The following carbon sources were tested: gelatin, maltose, glucose, fructose, galactose, arabinose, cellobiose, lactose, mannitol, mannose, rhamnose, sorbitol, sucrose, xylose, yeast extract, peptone and tryptone (each at 0·2 %, w/v); formate, pyruvate, propionate, butyrate, valerate, isovalerate, glutamate, caproate, caprylate, malate, succinate, isobutyrate, heptanoate, 2-methylbutyrate, 3-methylbutyrate, monomethylamine, acetate, lactate, propanol, ethanol and methanol (each at 10 mM, v/v). The strain was also characterized by using the API 20E identification system (bioMérieux) at 30 °C, according to the manufacter's instructions.
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and Lucas et al. (2002). Preparation of amorphous Fe(III) oxide and Fe(II) determination were performed as described earlier (Slobodkin et al., 1999). Compounds were considered to be electron acceptors if they supported growth of strain LT13aT on defined marine medium. Strain LT13aT used oxygen, nitrate, ferric iron, fumarate and cystine as terminal electron acceptors with lactate as the electron donor, but did not use trimethylamine-N-oxide, DMSO, manganese dioxide, thiosulphate, sulphite, tetrathionate, sulphate, elemental sulphur, molybdate, nitrite, succinate, glycine or carbon dioxide. Fermentation of various carbohydrates was tested by using modified YP medium from which carbon sources had been omitted. The following carbohydrates were tested: glucose, arabinose, cellobiose, fructose, galactose, lactose, maltose, mannitol, mannose, rhamnose, xylose, sucrose, sorbitol, Casamino acids, tryptone, peptone and yeast extract (each at 0·2 %, w/v), and pyruvate, lactate and malate (each at 10 and 30 mM).
Positive cultures were transferred twice (10 % inoculum) into the test media to confirm growth and were compared with the control cultures without the added carbon or electron acceptor. Growth observed within 48–72 h was considered as a positive result. The organic acid metabolic end products that were produced during fermentation of pyruvate were analysed by HPLC (Alliance 2690; Waters) as described by Wery et al. (2001).
For nitrite and ammonium analysis, cultures were grown anaerobically in solidified YP medium supplemented with 5 mM KNO3 and incubated at 37 °C. Reduction of nitrate and nitrite was determined by using the indophenol blue method of Koroleff (1969) and Solorzano (1969). H2S production was evaluated by adding 500 µl of a solution of CuSO4 (5 mM) and HCl (50 mM) to a 250 µl culture grown at 30 °C. The dark-brown precipitate, demonstrating the presence of sulphide, was compared with uninoculated medium incubated under the same conditions.
Respiratory lipoquinones and polar lipids were extracted from 100 mg freeze-dried cell material by using the two-stage method described by Tindall (1990a, b). Respiratory quinones were extracted by using methanol/hexane (Tindall, 1990b) and polar lipids were extracted by adjusting the remaining methanol/0·3 % aqueous NaCl phase (containing the cell debris) to give a chloroform/methanol/0·3 % aqueous NaCl mixture (1 : 2: 0·8, by vol.). The extraction solvent was stirred overnight and the cell debris was pelleted by centrifugation. Polar lipids were recovered into the chloroform phase by adjusting the chloroform/methanol/0·3 % aqueous NaCl mixture to a ratio of 1 : 1: 0·9 (by vol.).
Respiratory lipoquinones were separated into their different classes (menaquinones and ubiquinones) by TLC on silica gel (Macherey-Nagel; part no. 805023), using hexane/tert-butylmethylether (9 : 1, v/v) as solvent. UV-absorbing bands corresponding to menaquinones or ubiquinones were removed from the plate and further analysed by HPLC. This step was carried out on LDC Analytical HPLC equipment (Thermo Separation Products) fitted with a reverse-phase column (Macherey-Nagel; 2 mmx125 mm, 3 µm, RP18) using methanol as the eluent. Respiratory lipoquinones were detected at 269 nm.
The major respiratory quinones present comprised both ubiquinones and menaquinones. The major ubiquinones present were ubiquinone 7 (Q7) (21 %) and Q8 (79 %). The major menaquinones present were menaquinone 7 (MK7) (24 %), MK8 (1·7 %), monomethylmenaquinone 7 (MMK7) (70 %) and MMK8 (4·3 %). The presence of ubiquinones, menaquinones and methylmenaquinones has been reported in members of the genus Shewanella. The presence of Q7 and Q8 as the dominant ubiquinones, but also MK7 and MMK7 among the naphthoquinones, has previously been reported only in members of the genus Shewanella (Akagawa-Matsushita et al., 1992; Nogi et al., 1998; Venkateswaran et al., 1999; Bozal et al., 2002; Satomi et al., 2003).
Polar lipids were separated by two-dimentional silica-gel TLC (Macherey-Nagel; part no. 818135). The first direction was developed in chloroform/methanol/water (65 : 25 : 4, by vol.); the second was developed in chloroform/methanol/acetic acid/water (80 : 12 : 15 : 4, by vol.). Total lipid material and specific functional groups were detected by using dodecamolybdophosphoric acid (total lipids), Zinzadze reagent (phosphate), ninhydrin (free amino groups), periodic acid–Schiff stain (
-glycols), Dragendorff's reagent (quaternary nitrogen) and anisaldehyde/sulphuric acid (glycolipids).
Fatty acids were analysed as their methyl ester derivatives, which were prepared from 10 mg dry cell material. Cells were subjected to differential hydrolysis to detect ester-linked and non-ester-linked (amide-bound) fatty acids (B. J. Tindall, unpublished results). Fatty acid methyl esters were analysed by GC using a 0·2 µmx25 m non-polar capillary column and flame-ionization detection. The run conditions were as follows: injection and detector port temperature, 300 °C; inlet pressure, 60 kPa; split ratio, 50 : 1; injection volume, 1 µl; temperature program, 130–310 °C at a rate of 4 °C min–1.
The major polar lipids present were phosphatidylethanolamine and phosphatidylglycerol (see Supplementary Fig. C in IJSEM Online). Virtually no data are available on the polar lipid composition of Shewanella species, although unpublished work (G. Stöcklmair & B. J. Tindall) indicates that the presence of phosphatidylethanolamine and phosphatidylglycerol as the main phospholipids is not atypical of members of this genus. Furthermore, it would appear that both of these compounds resolve into subspots in the two-dimensional thin-layer chromatograms. This is in contrast to the polar lipids of Escherichia coli, for example, where the dominant compounds are also phosphatidylglycerol and phosphatidylethanolamine, but do not resolve into two spots (B. J. Tindall, unpublished results).
The fatty acids comprised straight-chain (saturated and unsaturated), branched-chain and hydroxy fatty acids (see Table 2 and Supplementary Table, available in IJSEM Online). These were predominantly 3-OH fatty acids, some of which were presumably amide-bound. Comparison with the fatty acid composition published previously indicates that the overall pattern is typical of members of this genus that have been examined to date. However, authors use different methods of analysing the fatty acids, so the results cannot be compared directly. On the basis of the fatty acid analyses reported previously by several authors, as well as the fact that much of the available literature is incomplete with respect to the presence of hydroxy fatty acids or 20 : 53c, we can only state that the fatty acid composition of strain LT13aT is based on all cellular components, including lipids and lipopolysaccharides and that mass spectrometry did not indicate that 20 : 53c was present. This is, to our knowledge, the first report in which the presence of both hydroxy fatty acids and 20 : 53c has been taken into consideration. The presence of hydroxy fatty acids, some of which appear to be amide-linked, is also consistent with the presence of a lipopolysaccharide and these components, though not always reported, may be of importance in differentiating members of the genus Shewanella (Makemson et al., 1997; Leonardo et al., 1999; Bozal et al., 2002; Brettar et al., 2002). Consistent with other reports on organisms similar to Shewanella putrefaciens, no polyunsaturated fatty acids (20 : 53c) were detected.
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. The G+C content of the genomic DNA was determined by HPLC according to the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ; Braunschweig, Germany). The genomic DNA G+C content of strain LT13aT is 44·9 mol%, a value in accordance with that of Shewanella species studied to date (Venkateswaran et al., 1999).
Sequencing reactions were performed by using a Thermo Sequenase primer cycle sequencing kit (Amersham Biosciences) and an automatic DNA analysis system (LI-COR 4000; Scientec) according to the manufacturers' protocols. A total of 1334 nt from the 16S rRNA gene was sequenced as described previously (Moore et al., 1995). Phylogenetic analysis was performed by using the software package ARB (Ludwig et al., 2004). Distance analysis [using the correction factor of Jukes & Cantor (1969)] and clustering with neighbour-joining (Saitou & Nei, 1987) and maximum-parsimony analysis (Lake, 1987) revealed that strain LT13aT affiliated within the genus Shewanella within the -Proteobacteria (Fig. 1). Strain LT13aT was related more closely to S. putrefaciens (98 % similarity), an environmental bacterium isolated from aquatic environments (Brettar & Höfle, 1993), sediments (Myers & Nealson, 1990) and oilfields (Semple & Westlake, 1987). Strain LT13aT was also related closely to Shewanella oneidensis (97 %) and Shewanella baltica (96 %). Strain LT13aT and S. putrefaciens clustered together in 98 and 70 % of bootstrap trees (by distance and parsimony, respectively) (Fig. 1).
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). DNA probes were labelled by using an enhanced chemifluorescence random-prime labelling kit (Amersham Biosciences). The level of hybridization is the mean level of binding for at least four replicates. The results of DNA–DNA hybridization experiments revealed that similarity for strain LT13aT was <20 % with the three closest reference strains (S. putrefaciens DSM 6067T, S. baltica DSM 9439T and S. oneidensis strain MR-1T), indicating that strain LT13aT is a novel species of Shewanella (Stackebrandt & Goebel, 1994).
When different taxonomic parameters were compared, strain LT13aT was found to differ from the Shewanella species that have been described (Table 1
). Strain LT13aT differs from its nearest phylogenetic neighbours as follows: (i) strain LT13aT was able to produce acetoin, amylase and ornithine decarboxylase, unlike S. putrefaciens, S. baltica or S. oneidensis; (ii) strain LT13aT can be distinguished from S. putrefaciens by means of gelatinase activity; (iii) strain LT13aT was able to use citrate as sole carbon source; (iv) strain LT13aT did not produce H2S from thiosulphate and elemental sulphur and did not reduce trimethylamine-N-oxide, but reduced cystine to H2S; (v) the optimal hydrostatic pressure for growth was 10 MPa; and (vi) levels of DNA similarity between strain LT13aT and the three closest neighbours were <20 %. On the basis of physiological properties, in combination with DNA–DNA hybridization with the closest described relatives, strain LT13aT represents a separate species within the genus Shewanella. Consequently, we propose to name this novel species Shewanella profunda sp. nov., with strain LT13aT as the type strain.
Description of Shewanella profunda sp. nov.
Shewanella profunda (L. fem. adj. profunda from the deep).
Cells are Gram-negative, rod-shaped and motile by means of a single polar flagellum. Facultatively anaerobic heterotroph. Oxidase-, amylase-, gelatinase-, ornithine decarboxylase- and acetoin-positive. No endospores or spores are formed. Colonies on agar are circular. Temperature range for growth is 4–37 °C (optimum growth occurs at 25–30 °C); pH range for growth is 6·5–8·0 (optimum, approx. pH 7·0); NaCl concentrations for growth are in the range 0–60 g l–1 (optimum, 5 g NaCl l–1). Hydrostatic pressure for growth is in the range 0·1–50 MPa at 30 °C (optimum, 10 MPa). Under optimal growth conditions, the doubling time of strain LT13aT is 45 min with agitation for a maximum cell density of 1x108 cells ml–1. Maltose, mannose, arabinose, sorbitol, succinate, glutamate, fumarate, citrate, lactate, pyruvate, yeast extract, peptone and tryptone are used as sole carbon and energy sources. Anaerobic growth occurs by fermentation of tryptone, peptone, yeast extract and pyruvate. Acids formed by fermentation of pyruvate are acetate, lactate and succinate. Strain LT13aT uses oxygen, nitrate, ferric iron, fumarate and cystine as terminal electron acceptors with lactate as electron donor. On the basis of 16S rRNA gene sequence analysis, the strain belongs to the -Proteobacteria and is a member of the genus Shewanella. Q7, Q8, MK7, MMK7 and MMK8 are present. Major polar lipids present are phosphatidylethanolamine and phosphatidylglycerol. Major fatty acids are 16 : 17c, 15 : 0 iso, 16 : 0 and 13 : 0 iso. Polyunsaturated fatty acids (e.g. 20 : 53c) are not present. The G+C content of the DNA is 44·9 mol%.
The type strain is LT13aT (=DSM 15900T=JCM 12080T) and was isolated from deep marine sediment at the Nankai Trough, off the coast of Japan in the Pacific Ocean (Ocean Drilling Program, Leg 190).
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ACKNOWLEDGEMENTS |
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