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1 Pacific Institute of Bioorganic Chemistry of the Far-Eastern Branch of the Russian Academy of Sciences, Pr. 100 Let Vladivostoku 159, 690022, Vladivostok, Russia
2 Tokyo Research Laboratories, Kyowa Hakko Kogyo Co. Ltd, 3-6-6 Asahi-machi, Machida-shi, Tokyo 194-8533, Japan
3 Institute of Marine Biology of the Far-Eastern Branch of the Russian Academy of Sciences, Pal'chevskogo St 17, 690032, Vladivostok, Russia
Correspondence
Makoto Suzuki
makoto.suzuki{at}kyowa.co.jp
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15 : 0 (68·8 and 8·4 %, respectively). On the basis of phenotypic, chemotaxonomic, genotypic and phylogenetic characteristics, the novel bacterium has been designated Vitellibacter vladivostokensis gen. nov., sp. nov. The type strain is KMM 3516T (=NBRC 16718T).
The GenBank accession number for the 16S rDNA sequence of Vitellibacter vladivostokensis KMM 3516T is AB071382.
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; Barbeyron et al., 2000; Humphry et al., 2001; Politz et al., 2000). Members of genera such as Cellulophaga, Tenacibaculum and Flavobacterium may be free-living or host-associated organisms (Johansen et al., 1999; Suzuki et al., 2001; McCammon & Bowman, 2000). Recently, we reported the isolation of a new representative of the CFB phylum, Arenibacter latericius gen. nov., sp. nov. (Ivanova et al., 2001), strains of which were found in bottom sediment samples collected in the South China Sea, on the fronds of the brown alga grown in the Kuril Isles region (Sea of Okhotsk) and in the edible holothurian Apostichopus japonicus, which inhabits the coastal waters of the Sea of Japan. According to phylogenetic analysis, the genus Arenibacter forms single cluster with representatives of the recently described genera Muricauda and Zobellia (Bruns et al., 2001; Barbeyron et al., 2001). The latter accommodates two species, Zobellia uliginosa (formerly Cellulophaga uliginosa; Bowman, 2000) and Zobellia galactanivorans (Barbeyron et al., 2001). In the present work, we examined by polyphasic taxonomy another environmental isolate associated with the holothurian Apostichopus japonicus, and found a novel bacterium belonging to the CFB phylum and closely related to the Arenibacter–Zobellia–Muricauda phylogenetic cluster. Based on polyphasic taxonomy data (phylogenetic, pheno- and genotypic analyses, menaquinone and cellular fatty acid compositions) obtained and presented in this work, we describe a new member of the family Flavobacteriaceae, Vitellibacter vladivostokensis gen. nov., sp. nov.
Strain KMM 3516T was isolated from gut of the holothurian Apostichopus japonicus collected in Troitsa Bay, in the Gulf of Peter the Great (Sea of Japan) in November 1997 from a depth of 8 m (salinity 33 
, temperature 12 °C). For strain isolation 0·1 ml tissue homogenates was transferred on to plates of Marine agar 2216 (Difco). After primary isolation and purification strain KMM 3516T was cultivated at 28 °C on the same medium and stored at -80 °C in Marine broth (Difco) supplemented with 20 % (v/v) glycerol.
Oxidative or fermentative utilization of glucose was determined on the Hugh & Leifson medium modified for marine bacteria (Lemos et al., 1985). Catalase activity was tested by addition of 3 % (v/v) H2O2 solution to a bacterial colony and observed for the appearance of gas. Flexirubin pigments were examined by Fautz & Reichenbach (1980) method. Gram-staining, degradation of alginic acids (1 %, w/v) and agar (1·5 %, w/v), oxidase and alkaline phosphatase activity, production of acid from carbohydrates, hydrolysis of starch, casein, gelatin, cellulose (filter paper), Tween 20, Tween 40, Tween 80, DNA and urea, nitrate reduction, production of hydrogen sulphide and indole were carried out according to the methods of Smibert & Krieg (1994). Hydrolyses of chitin (1 %, w/v), elastin (2 %, w/v) and CM-cellulose (1 %, w/v) were tested by appearance of clear zones around colonies. A medium containing 0·2 g NaNO3, 0·2 g NH4Cl, 0·05 g Yeast Extract (Difco) and 0·4 % (w/v) carbon source in 1 l artificial sea water was used to examine carbon-source utilization. Carbon sources tested were arabinose, glucose, lactose, mannose, sucrose, inositol, sorbitol, mannitol, glycerol, N-acetylglucosamine, acetate, citrate, malonate, tartrate and alanine. In order to study of the temperature range, bacteria were cultivated on medium A, which contained (l-1) 5 g Bacto peptone (Difco), 2 g Bacto yeast extract (Difco), 1 g glucose, 0·02 g KH2PO4 and 0·05 g MgSO4.7H2O in 50 % (v/v) natural sea water and 50 % (v/v) distilled water. Bacterial growth at the different concentrations of NaCl was checked on the medium A prepared with distilled water and containing 0, 1, 2, 3, 5, 6, 8, 10 and 12 % (w/v) of NaCl. Spreading growth was observed by cultivation on the medium B, which contained (l-1) 1 g Bacto peptone, 1 g yeast extract, 15 g agar and half-strength natural sea water under high moisture conditions. Gliding motility was determined as described by Bowman (2000). The cell movement at the edges of colony was verified by using phase-contrast microscopy. Susceptibility to antibiotics was examined by the routine diffusion plate method. Disks were impregnated with the following antibiotics: ampicillin (10 µg), benzylpenicillin (10 µg), carbenicillin (100 µg), gentamicin (10 µg), kanamycin (30 µg), lincomycin (15 µg), neomycin (30 µg), oleandomycin (15 µg), polymyxin B (300 U), streptomycin (10 µg), tetracycline (30 µg).
To determine fatty acid composition, strains were cultivated at 28 °C for 72 h on medium A. The analysis of fatty acid methyl esters was performed by GLC [30 mx0·25 mm Supelcowax 10 column, 205 °C] as described by Svetashev et al. (1995). Isoprenoid quinones were extracted and analysed by the method of Nakagawa & Yamasato (1993).
DNA was isolated following the method of Marmur (1961) and the DNA G+C content was determined by the thermal denaturation method (Marmur & Doty, 1962). The 16S rDNA gene sequence of KMM 3516T was determined by PCR amplification and direct sequencing (Hiraishi, 1992). Conditions and reagents used for PCR amplification and sequencing of 16S rDNA were described previously (Suzuki et al., 2001). The determined sequence was aligned to the alignment based on secondary structure model which is maintained by the SSU rRNA database (Van de Peer et al., 2000) using the profile alignment program of CLUSTAL W software (Thomson et al., 1994). The evolutionary distances were then computed with the DNADIST program in the PHYLIP 3.572 package (Felsenstein, 1995) with the Kimura 2-parameter model (Kimura, 1980), and the phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987). To evaluate the phylogenetic trees, a bootstrap analysis with 1000 sample replications was performed with the SEQBOOT and CONSENSE programs in the PHYLIP 3.572 package. The phylogenetic position of KMM 3516T was also verified by maximum-parsimony analysis using the PAUP version 3.1.1 program and by maximum-likelihood analysis using DNAML program in the PHYLIP 3.572 package.
Strain KMM 3516T was Gram-negative, chemo-organotrophic with respiratory type of metabolism, non-motile by gliding, asporogenic and consisted of single flexible rods, 0·3–0·5 µm in diameter and 3–10 µm long. On marine agar, colonies were round, 2–4 mm in diameter, yellow-orange-pigmented, shiny and convex, with entire margins. It was oxidase-, catalase- and alkaline phosphatase-positive, and required Na+ ions for growth. Growth occurred on media containing 1–6 % (w/v) NaCl (optimum 2 %). The temperature range for growth was 4–43 °C (optimum 28 °C). The pH range of growth was 5·5–10·0 (optimum 7·5–8·5). Flexirubin pigments were formed. Gelatin, casein, elastin, Tween 20, Tween 40 and DNA were degraded. Cellulose (CM-cellulose and filter paper), chitin, agar, starch, alginate, urea, Tween 60 and Tween 80 were not hydrolysed. H2S and indole were not produced. No acid was formed from arabinose, cellobiose, fucose, galactose, glucose, lactose, maltose, melibiose, raffinose, rhamnose, sorbose, sucrose, xylose, adonitol, dulcitol, glycerol, inositol, mannitol, sorbitol, N-acetylglucosamine or citrate. Glycerol, N-acetylglucosamine, acetate, citrate, malonate, tartrate and alanine were utilized, whereas arabinose, glucose, lactose, mannose, sucrose, inositol, mannitol and sorbitol were not. Nitrate reduction was negative. Strain KMM 3516T was susceptible to carbenicillin, oleandomycin and lincomycin, but not to ampicillin, benzylpenicillin, streptomycin, gentamicin, neomycin, polymyxin B or tetracycline.
The whole-cell fatty acid composition of KMM 3516T is shown in Table 1. The predominant cellular fatty acids were branched-chain saturated, namely i15 : 0 (68·8 %) and 15 : 0 (8·4 %) fatty acids. The major isoprenoid quinone was menaquinone MK-6. The G+C content of the genomic DNA of strain KMM 3516T was 41·3 mol%.
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). Also the bootstrap probability of this lineage was low, but the clustering of KMM 3516T and genera Arenibacter and Zobellia was shown in other analyses using maximum-parsimony and maximum-likelihood methods. In these analysis the genus Cellulophaga was always monophyletic and the nearest genus to the lineage of KMM 3516T – genera Arenibacter and Zobellia. It is evident from the tree that KMM 3516T represents a distinct sublineage within the family Flavobacteriaceae.
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) and forms a distinct lineage within cluster represented by Arenibacter latericius, Zobellia galactanivorans, Zobellia uliginosa, Muricauda ruestringensis and strain ACAM 210, with sequence similarities of 90·0, 90·0, 90·1, 90·1 and 89·8 %, respectively. The values of the level of 16S rDNA sequence similarities of KMM 3516T with other members of the CFB were only 78·6–90·1 %. The large phylogenetic distance of the novel marine environmental isolate from related genera of the CFB group described to date clearly demonstrates that strain KMM 3516T represents a new genus.
The main differential phenotypic traits of strain KMM 3516T and members of other allied marine taxa are shown in Table 2. It is distinguished from the genus Arenibacter by the presence of flexirubin pigments and high DNA G+C content. KMM 3516T and members of the genus Zobellia have similar characteristics in common, but Zobellia species are agarolytic and motile by gliding. The absence of the gliding motility, flexirubin production, starch and agar hydrolysis differentiates KMM 3516T from Cellulophaga species. Strain KMM 3516T differs from M. ruestringensis by respiratory metabolism, catalase, gelatinase and flexirubin production, and absence of gliding motility. Gliding motility was never observed for strain KMM 3516T under any culture conditions used. KMM 3516T is distinguished from the Psychroflexus species by the presence of flexirubin pigments, ability to grow at 43 °C and absence of starch hydrolysis. Strain KMM 3516T is clearly differentiated from the genera Salegentibacter, Polaribacter, Tenacibaculum, Gelidibacter and Psychroserpens by several phenotypic traits including the presence of flexirubin pigments, oxidase activity, gliding motility, growth temperature, nitrate reduction and higher DNA G+C content (Table 2).
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) were examined. The strains tested were grown under the same conditions (nutrient medium composition, period and temperature of cultivation) because of the results of cellular fatty acid analysis often depend on the growth conditions (Kaneda, 1991; Barbeyron et al., 2001; Männistö & Puhakka, 2001). The whole-cell fatty acid data show that KMM 3516T has similar cellular fatty acid composition with members of the family Flavobacteriaceae, but its fatty acid profile differs significantly from other phylogenetic relatives. As shown in Table 1, KMM 3516T contains i15 : 0 and 15 : 0 as its major fatty acids, but has much more i15 : 0 (68·8 %) in comparison with the genera Arenibacter, Tenacibaculum and Flavobacterium (16·0, 19·6 and 7·3 %, respectively). Strain KMM 3516T can be differentiated from members of the genera Arenibacter, Zobellia, Salegentibacter, Cellulophaga and Flavobacterium by the amount of 16 : 1
7 (0·1 and 12·4, 10·1, 6·0, 4·9, 14·3 %, respectively). The level of i15 : 0-2-OH of the genus Salegentibacter is 29·3 % in contrast to the other above-mentioned genera and KMM 3516T which contained <2·1 %. Low value of i17 : 0-3-OH fatty acid differs holothurian isolate from representatives of the genera Arenibacter and Cellulophaga. Of particular interest is the fact that cells of KMM 3516T contain 93·4 % branched fatty acids in contrast to its close phylogenetic neighbours A. latericius KMM 426T and Z. uliginosa CIP 104808T (61·8 % and 60·7 %, respectively). The results of the polyphasic taxonomic analysis indicate that strain KMM 3516T does not belong to any of the other taxa currently included in the CFB phylum. Thus, we propose that strain KMM 3516T be classified as Vitellibacter vladivostokensis gen. nov., sp. nov.
Description of Vitellibacter gen. nov.
Vitellibacter (Vi.tel.li.bac'ter. L. n. vitellus egg yolk; N.L. masc. n. bacter rod; N.L. masc. n. Vitellibacter egg-yolk-coloured rod).
Rod-shaped cells, not flagellated, no gliding motility. Gram-negative. Do not form endospores. Requires Na+ ions for growth. Strictly aerobic. Produces non-diffusible yellow-orange pigments. Flexirubins are synthesized. Chemo-organotrophic. Cytochrome oxidase-, catalase- and alkaline phosphatase-positive. The major respiratory quinone is MK-6. The main cellular fatty acids are branched-chain saturated fatty acids i15 : 0 and 15 : 0. As determined by 16S rDNA sequence analysis, the genus Vitellibacter is a member of the Cytophaga–Flavobacterium–Bacteroides phylum, family Flavobacteriaceae. The type species is Vitellibacter vladivostokensis.
Description of Vitellibacter vladivostokensis sp. nov.
Vitellibacter vladivostokensis (vla.di.vo.sto.ken'sis. N.L. adj. vladivostokensis pertaining to Vladivostok, a city in Asian Russia, where the organism was first isolated).
Main characteristics are otherwise the same as those given for genus. In addition, cells are 0·3–0·5 µm wide and 3–10 µm long. Colonies are 2–4 mm in diameter, circular, shiny, convex, with entire edges on solid media containing high nutrient components. Growth occurs at 4–43 °C. Optimal temperature for growth is 28 °C. Growth is detected at 1–6 % NaCl. Decomposes gelatin, casein, DNA, elastin, Tween 20 and Tween 40. Do not hydrolyse cellulose (CM-cellulose and filter paper), chitin, agar, starch, alginate, urea, Tween 60 and Tween 80. Does not form acid from arabinose, cellobiose, fucose, galactose, glucose, lactose, maltose, melibiose, raffinose, rhamnose, sorbose, sucrose, xylose, adonitol, dulcitol, glycerol, inositol, mannitol, sorbitol, N-acetylglucosamine or citrate. Glycerol, N-acetylglucosamine, acetate, citrate, malonate, tartrate and alanine are utilized. Arabinose, glucose, lactose, mannose, sucrose, inositol, mannitol and sorbitol are not utilized. Nitrate is not reduced to nitrite. H2S and indole production are negative. The G+C content of the DNA is 41·3 mol%.
The type strain is deposited in Collection of Marine Microorganisms (KMM) of Pacific Institute of Bioorganic Chemistry of Far-Eastern Branch of Russian Academy of Sciences, Vladivostok, Russia, as KMM 3516T, and in NITE Biological Resource Center (formerly Institute for Fermentation Osaka; IFO), Chiba, Japan, as NBRC 16718T; isolated from the holothurian Apostichopus japonicus, collected in Troitsa Bay in the Gulf of Peter the Great (Sea of Japan).
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K. W. K. Lau, C. Y. M. Ng, J. Ren, S. C. L. Lau, P.-Y. Qian, P.-K. Wong, T. C. Lau, and M. Wu Owenweeksia hongkongensis gen. nov., sp. nov., a novel marine bacterium of the phylum 'Bacteroidetes' Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1051 - 1057. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, K. H. Lee, K. S. Bae, G. M. Frolova, V. V. Mikhailov, and I. S. Kim Pibocella ponti gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi Int J Syst Evol Microbiol, January 1, 2005; 55(1): 177 - 181. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, G. M. Frolova, V. V. Mikhailov, K. H. Lee, and K. S. Bae Description of Aquimarina muelleri gen. nov., sp. nov., and proposal of the reclassification of [Cytophaga] latercula Lewin 1969 as Stanierella latercula gen. nov., comb. nov. Int J Syst Evol Microbiol, January 1, 2005; 55(1): 225 - 229. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, V. V. Mikhailov, K. S. Bae, and I. S. Kim Salegentibacter mishustinae sp. nov., isolated from the sea urchin Strongylocentrotus intermedius Int J Syst Evol Microbiol, January 1, 2005; 55(1): 235 - 238. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, K. H. Lee, V. V. Mikhailov, and K. S. Bae Gillisia mitskevichiae sp. nov., a novel bacterium of the family Flavobacteriaceae, isolated from sea water Int J Syst Evol Microbiol, January 1, 2005; 55(1): 321 - 323. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, A. M. Lysenko, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Bizionia paragorgiae gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the soft coral Paragorgia arborea Int J Syst Evol Microbiol, January 1, 2005; 55(1): 375 - 378. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, S. K. Han, A. M. Lysenko, M. Rohde, M.-S. Rhee, G. M. Frolova, E. Falsen, V. V. Mikhailov, and K. S. Bae Maribacter gen. nov., a new member of the family Flavobacteriaceae, isolated from marine habitats, containing the species Maribacter sedimenticola sp. nov., Maribacter aquivivus sp. nov., Maribacter orientalis sp. nov. and Maribacter ulvicola sp. nov. Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1017 - 1023. [Abstract] [Full Text] [PDF]
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J.-C. Cho and S. J. Giovannoni Robiginitalea biformata gen. nov., sp. nov., a novel marine bacterium in the family Flavobacteriaceae with a higher G+C content Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1101 - 1106. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, S. K. Han, M.-S. Rhee, A. M. Lysenko, M. Rohde, N. V. Zhukova, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Algibacter lectus gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from green algae Int J Syst Evol Microbiol, July 1, 2004; 54(4): 1257 - 1261. [Abstract] [Full Text] [PDF]
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S. Van Trappen, I. Vandecandelaere, J. Mergaert, and J. Swings Gillisia limnaea gen. nov., sp. nov., a new member of the family Flavobacteriaceae isolated from a microbial mat in Lake Fryxell, Antarctica Int J Syst Evol Microbiol, March 1, 2004; 54(2): 445 - 448. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, S. B. Kim, S. K. Han, M. S. Rhee, A. M. Lysenko, E. Falsen, G. M. Frolova, V. V. Mikhailov, and K. S. Bae Ulvibacter litoralis gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the green alga Ulva fenestrata Int J Syst Evol Microbiol, January 1, 2004; 54(1): 119 - 123. [Abstract] [Full Text] [PDF]
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O. I. Nedashkovskaya, M. Suzuki, M. V. Vysotskii, and V. V. Mikhailov Arenibacter troitsensis sp. nov., isolated from marine bottom sediment Int J Syst Evol Microbiol, September 1, 2003; 53(5): 1287 - 1290. [Abstract] [Full Text] [PDF]
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