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1 School of Earth and Environmental Sciences and Research Institute of Oceanography, Seoul National University, San 56-1 Shillim-dong, Kwanak-gu, Seoul 151-742, Republic of Korea
2 School of Biological Sciences, Seoul National University, San 56-1 Shillim-dong, Kwanak-gu, Seoul 151-742, Republic of Korea
Correspondence
Byung Cheol Cho
bccho{at}snu.ac.kr
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ABSTRACT |
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7c and/or iso-C15 : 0 2-OH, 19·6 %), iso-C15 : 0 (18·8 %) and iso-C17 : 0 3-OH (13·6 %). Fatty acids such as C18 : 36c (6,9,12) (1·5 %) and summed feature 4 (iso I- and/or anteiso B-C17 : 1, 1·3 %) were uniquely found in minor quantities in CL-TF13T among Tenacibaculum species. The DNA G+C content was 30 mol%. According to physiological data, fatty-acid composition and 16S rRNA gene sequence, CL-TF13T could be assigned to the genus Tenacibaculum but distinguished from the recognized species of the genus. Therefore, strain CL-TF13T (=KCCM 42115T=JCM 13039T) represents a novel species, for which the name Tenacibaculum litoreum sp. nov. is proposed.
Published online ahead of print on 4 November 2005 as DOI 10.1099/ijs.0.64044-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain CL-TF13T is AY962294.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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, six species have been isolated from various marine sources. Two species, Tenacibaculum maritimum and Tenacibaculum ovolyticum, were reclassified from the former [Flexibacter] maritimus isolated from diseased red sea bream fingerling (Wakabayasahi et al., 1986) and [Flexibacter] ovolyticus isolated from halibut egg (Hansen et al., 1992). Two other species, Tenacibaculum mesophilum and Tenacibaculum amylolyticum, were isolated from homogenates of sponge and surfaces of marine macroalgae, respectively (Suzuki et al., 2001). Tenacibaculum skagerrakense and Tenacibaculum lutimaris were recently isolated from sea water (Frette et al., 2004) and tidal flat sediment (Yoon et al., 2005), respectively. In this study, strain CL-TF13T, related to the genus Tenacibaculum, was isolated from tidal flat sediment in Ganghwa, Korea. The sediment slurry was spread onto a plate containing marine agar 2216 (MA; Difco) and the plate was incubated at 30 °C for 1 week. Strain CL-TF13T was isolated on the plate and subsequently purified four times on MA at 30 °C. The strain was maintained both on MA at 4 °C and in marine broth 2216 (MB; Difco) supplemented with 30 % (v/v) glycerol at –80 °C.
The 16S rRNA gene was amplified from a single colony by PCR with Taq DNA polymerase (Bioneer) and primers 27F and 1492R (Lane, 1991). The PCR product was purified using the AccuPrep PCR Purification kit (Bioneer) and cloned using the pCR2.1 TOPO TA Cloning kit (Invitrogen). Sequencing of the 16S rRNA gene was performed with an Applied Biosystems automatic sequencer (ABI 3730XL) at Macrogen (Seoul, Korea). The almost-complete 16S rRNA gene sequence of strain CL-TF13T (1446 bp) was obtained and compared with 16S rRNA gene sequences available in GenBank using BLASTN (Altschul et al., 1990) searches. The sequence of strain CL-TF13T was manually aligned with those of the type strains of six Tenacibaculum species and with the type species of other genera in the family Flavobacteriaceae obtained from GenBank and Ribosomal Database Project (Cole et al., 2003) databases using known 16S rRNA secondary structure information. Phylogenetic trees were obtained by neighbour-joining (Saitou & Nei, 1987), maximum-parsimony (Fitch, 1971) and maximum-likelihood (Felsenstein, 1981) methods. An evolutionary distance matrix for the neighbour-joining method was generated according to the model of Jukes & Cantor (1969). The robustness of tree topologies was assessed by bootstrap analyses based on 1000 replications for neighbour-joining and maximum-parsimony methods and 100 replications for the maximum-likelihood method. Alignment analysis was carried out using the jPHYDIT program (version 1.0; http://chunlab.snu.ac.kr/jphydit/) and phylogenetic analysis was carried out using MEGA3 (Kumar et al., 2004) and PAUP* 4.0 (Swofford, 1998). Likelihood parameters were estimated by the hierarchical ratio tests in MODELTEST, version 3.04 (Posada & Crandall, 1998). Sequence similarity indicated that the closest relatives of strain CL-TF13T were T. lutimaris (97·4 %), T. mesophilum (97·1 %), T. skagerrakense (96·5 %), T. amylolyticum (96·0 %), T. ovolyticum (95·4 %) and T. maritimum (94·2 %). Phylogenetic analyses based on the 16S rRNA gene sequence showed that strain CL-TF13T formed a robust cluster with species of the genus Tenacibaculum (Fig. 1). Thus, it is clear that our isolate belongs to the genus Tenacibaculum. The DNA G+C content was determined using the thermal denaturation method (Mandel & Marmur, 1968) and was found to be 30 mol%, at the lower limit of the range reported in other Tenacibaculum species (Table 1). As the similarities between strain CL-TF13T and two species (T. lutimaris and T. mesophilum) were close to the theoretical threshold (97 %) for the delineation of bacterial species based on 16S rRNA gene sequence similarity (Stackebrandt & Goebel, 1994), the relatedness of genomic DNA was determined by dot-blot hybridization. Probe DNA labelling was performed using a nick translation kit (Roche) and hybridization and detection were done using the DIG labelling and detection kit (Roche) according to the manufacturer's instruction. The DNA–DNA relatedness between CL-TF13T and T. lutimaris was 11 %, while that for T. mesophilum was 46 %. These values are below the currently accepted limit of DNA relatedness (70 %) for the phylogenetic definition of a species (Stackebrandt & Goebel, 1994) and therefore provide evidence that the isolate represents a novel species in the genus Tenacibaculum.
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. Cell morphology was examined by phase-contrast microscopy and transmission electron microscopy (JEOL EX2) with cells grown at 30 °C in MB. Gliding motility was observed by the hanging-drop method (Suzuki et al., 2001). Anaerobic growth was checked on MA using the GasPak anaerobic system (BBL). Catalase and oxidase activities were determined according to the protocols described by Smibert & Krieg (1994), and gelatinase, amylase, DNase and nitrate reductase activities and degradation of Tween 80 were examined as described by Hansen & Sørheim (1991). Cells are rod-shaped (Fig. 2) and motile by means of gliding. Spherical cells were rarely observed in ageing cultures of CL-TF13T (Fig. 2b). Colony size, shape and colour were determined on MA after 5 days incubation at 30 °C. Colonies were pale yellow in colour, greenish glistening and irregular with spreading edges on MA. Colonies were 5–10 mm in diameter and not adherent to the agar. Other morphological characteristics are shown in Table 1
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-galactosidase, acid production from glucose and hydrolysis of aesculin were tested using API 20NE kit (bioMérieux) according to the manufacturer's instruction, except that the cell suspension was prepared using artificial sea water (ASW; 24 g NaCl, 5·1 g MgCl2, 4 g Na2SO4, 1·1 g CaCl2, 0·7 g KCl, 0·2 g NaHCO3, 0·1 g KBr, 0·027 g H3BO3, 0·024 g SrCl2, 0·003 g NaF, 1 l distilled water; Lyman & Fleming, 1940) as a suspension medium. Other enzyme activities were also assayed by using the API ZYM kit (bioMérieux) and ASW as a suspension medium. Carbon utilization was tested on basal medium agar (0·2 g NH4Cl, 0·2 g NaNO3, 0·05 g yeast extract, 15 g Bacto agar, 1 l ASW) containing 0·4 % of the carbon source. Incubation was prolonged for 1 month and growth was scored as negative when growth was equal to or less than that in the negative control, without any carbon source. For the analyses of API 20NE, API ZYM and carbon utilization tests, T. lutimaris TF-26T and T. maritimum NCIMB 2514T were employed as reference strains. In contrast to the other Tenacibaculum species, CL-TF13T grew optimally at 35–40 °C and was able to grow at pH 10, with 3–5 % (w/v) NaCl and with 1–10 % (w/v) sea salts (Table 1). The strain showed positive responses in tests for nitrate reductase, gelatinase, DNase, amylase, catalase, cytochrome oxidase and degradation of Tween 80 (Table 1). The other results of biochemical and physiological tests are given in Table 1 and the species description.
Isoprenoid quinone was isolated according to Minnikin et al. (1984) and analysed by HPLC as described by Collins (1985). The major isoprenoid quinone in CL-TF13T was menaquinone-6 (MK-6). Pigments were extracted from cells cultured in the dark for 1 day by using methanol and analysed by HPLC system. Flexirubin pigments were detected by a colour-shift test using 20 % (w/v) KOH solution (Reichenbach, 1992). CL-TF13T contained zeaxanthin as the major carotenoid pigment but did not contain flexirubin pigments. Thus, the characteristics of isoprenoid quinone and pigments were the same as other Tenacibaculum species. The fatty acid methyl esters in whole cells, which were grown on MA at 30 °C for 1 day, were analysed by gas chromatography according to the instructions of the Microbial Identification system (MIDI) at the Korean Culture Center of Microorganisms (Seoul, Korea). Similar to other members of the genus, the fatty-acid profile of CL-TF13T was dominated by summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH, 19·6 %), iso-C15 : 0 (18·8 %), iso-C17 : 0 3-OH (13·6 %), iso-C15 : 1 (8·2 %), iso-C16 : 0 3-OH (6·8 %) and iso-C15 : 0 3-OH (6·6 %) (Table 2). However, the relative proportions of the dominant fatty acids in CL-TF13T were different from other Tenacibaculum species and three fatty acids, C18 : 36c (6,9,12) (1·5 %), summed feature 4 (iso I- and/or anteiso B-C17 : 1, 1·3 %) and an unknown fatty acid (ECL 13.565) (1·3 %), were uniquely found in minor quantities in CL-TF13T among Tenacibaculum species. Therefore, the fatty-acid pattern of strain CL-TF13T differed significantly from those of previously described Tenacibaculum species.
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Description of Tenacibaculum litoreum sp. nov.
Tenacibaculum litoreum (li.to.re'um. L. neut. adj. litoreum of the shore).
Gram-negative, strictly aerobic and straight rods, approximately 0·3–0·5x2–35 µm in size. Cells are motile by means of gliding. On MA solid medium colonies are pale yellow, irregular with spreading edges and greenish glistening. After 5 days on MA at 30 °C colonies are approximately 5–10 mm in diameter. Growth occurs within the temperature range of 5–40 °C (optimum 35–40 °C) and at pH values of 6–10. Growth occurs in NaCl concentrations of 3–5 % (w/v) and in sea salt concentrations of 1–10 % (w/v). Positive for catalase, cytochrome oxidase, amylase, gelatinase, DNase and nitrate reductase and degradation of Tween 80. Major fatty acids are summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH, 19·6 %), iso-C15 : 0 (18·8 %) and iso-C17 : 0 3-OH (13·6 %). Also contains minor amounts of C18 : 36c (6,9,12) (1·5 %) and summed feature 4 (iso I- and/or anteiso B-C17 : 1, 1·3 %). According to API 20NE tests, activities for nitrate reductase and gelatinase are present, whereas activities for indole production, acid production from glucose, arginine dihydrolase and urease, hydrolysis of aesculin and -galactosidase are absent. According to API ZYM tests, activities for alkaline phosphatase, esterase (C4 and C8), leucine arylamidase, valine arylamidase, cystine arylamidase, trypsin, 
-chymotrypsin, acid phosphatase and naphthol-AS-BI-phosphohydrolase are present, whereas activities for lipase (C14), -galactosidase, -galactosidase, -glucuronidase, -glucosidase, -glucosidase, N-acetyl--glucosaminidase, -mannosidase and -fucosidase are absent. Growth occurs on Casamino acids, tryptone, yeast extract, peptone, L-arginine, L-ornithine, L-proline and L-lysine. No growth occurs on acetate, benzoate, citrate, maleic acid, ethanol, glycerol, L-leucine, tartrate, pyruvic acid, succinate, sucrose, L-glutamate, D-ribose, DL-aspartate, N-acetylglucosamine, L-arabinose, D-xylose, D-fructose, D-glucose, D-mannose, D-trehalose, inulin, D-mannitol, D-sorbitol, D-salicin, D-raffinose, D-galactose, urea or lactose. The DNA G+C content is 30 mol%.
The type strain, CL-TF13T (=KCCM 42115T=JCM 13039T), was isolated from a tidal flat sediment in Ganghwa, Korea.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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Cole, J. R., Chai, B., Marsh, T. L. & 8 other authors (2003). The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31, 442–443.
Collins, M. D. (1985). Analysis of isoprenoid quinones. Methods Microbiol 18, 329–366.
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Frette, L., Jørgensen, N. O. G., Irming, H. & Kroer, N. (2004). Tenacibaculum skagerrakense sp. nov., a marine bacterium isolated from the pelagic zone in Skagerrak, Denmark. Int J Syst Evol Microbiol 54, 519–524.
Hansen, G. H. & Sørheim, R. (1991). Improved method for phenotypical characterization of marine bacteria. J Microbiol Methods 13, 231–241.
Hansen, G. H., Bergh, Ø., Michaelsen, J. & Knappskog, D. (1992). Flexibacter ovolyticus sp. nov., a pathogen of eggs and larvae of Atlantic halibut, Hippoglossus hippoglossus L. Int J Syst Bacteriol 42, 451–458.
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