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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 Korean Collection for Type Cultures, Biological Resources Center, Korea Research Institute of Bioscience and Biotechnology, Yusong, Daejon 305-333, Republic of Korea
3 Institute of Microbiology of the Russian Academy of Sciences, Pr. 60 Let October 7/2, Moscow, 117811, Russia
4 Culture Collection, Department of Clinical Bacteriology, University of Göteborg, Guldhedsgatan 10, S-413 46 Göteborg, Sweden
Correspondence
Olga I. Nedashkovskaya
olganedashkovska{at}piboc.dvo.ru
or olganedashkovska{at}yahoo.com
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ABSTRACT |
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Published online ahead of print on 4 July 2003 as DOI 10.1099/ijs.0.02757-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Ulvibacter litoralis KMM 3912T is AY243096.
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; Bano & Hollibaugh, 2002; Kirchman, 2002). Despite broad application of molecular techniques to bacterial identification, study of the phenotypic properties of micro-organisms is essential for species discrimination (Vandamme et al., 1996). For example, the presence of cell-bound flexirubin-type pigments is considered to be an important phenotypic characteristic for differentiation of the bacteria of the CFB phylum from each other and from other Gram-negative, non-motile micro-organisms (Fautz & Reichenbach, 1980). Six species of marine representatives of the CFB phylum, namely Chryseobacterium indoltheticum, Chryseobacterium scophthalmum, Zobellia galactanivorans, Zobellia uliginosa, Reichenbachia agariperforans and Vitellibacter vladivostokensis, are currently known to be flexirubin-type pigment producers; they demonstrate a colony colour shift from yellow or orange to red, brown or purple after addition of 20 % KOH (Reichenbach, 1989; Vandamme et al., 1994; Barbeyron et al., 2001; Nedashkovskaya et al., 2003a, b). During the investigation of taxonomic diversity of the microbial population of the common green alga Ulva fenestrata from the Sea of Japan, novel flexirubin-producing bacteria were isolated. Phylogenetic analysis based on 16S rDNA sequencing revealed that strain KMM 3912T forms a cluster with representatives of the genera Cellulophaga, Arenibacter, Zobellia, Muricauda, Aequorivita and Vitellibacter and with [Cytophaga] marinoflava, in which it occupies a distinct lineage. The polyphasic taxonomic study presented in this work, which includes characterization of the phenotypic, chemotaxonomic and genotypic characteristics of strains KMM 3912T and KMM 3976 in combination with phylogenetic differences, supports the creation of a novel genus; we therefore describe a novel member of the family Flavobacteriaceae, designated Ulvibacter litoralis gen. nov., sp. nov.
Strains KMM 3912T and KMM 3976 were isolated from samples of the green alga Ulva fenestrata that were collected in Troitsa Bay, Gulf of Peter the Great, Sea of Japan, during June 2000. For strain isolation, 0·1 ml homogenates of algal fronds were transferred onto plates of marine agar 2216 (Difco). After primary isolation and purification, strains were 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 by using the medium of Hugh & Leifson, 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 observation for the appearance of gas. Flexirubin pigments were detected by using the method of Fautz & Reichenbach (1980). Gram-staining reaction, degradation of alginic acids (1 %, w/v) and agar (1·5 %, w/v), oxidase, urease, alkaline phosphatase and 
-galactosidase activities, production of acid from carbohydrates, hydrolysis of starch, casein, gelatin, cellulose (filter paper and CM-cellulose), chitin, Tweens 20, 40 and 80 and DNA, nitrate reduction and production of hydrogen sulphide and indole were carried out according to methods described by Smibert & Krieg (1994). To examine carbon source utilization, commercial API 20NE identification strips (bioMérieux) were used, following the instructions of the manufacturers, with a medium that contained 0·2 g NaNO3, 0·2 g NH4Cl, 0·05 g yeast extract (Difco) and 0·4 % (w/v) carbon source in 1000 ml artificial sea water. In order to study the temperature range for growth, bacteria were cultivated on medium A, which consisted of (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 different concentrations of NaCl was checked on medium A that was prepared with distilled water and contained 0, 1, 2, 3, 5, 6, 8, 10 or 12 % (w/v) NaCl. Spreading growth was observed by cultivation on medium B, which contained (l-1): 1 g Bacto peptone (Difco), 1 g yeast extract (Difco), 15 g agar and half-strength natural sea water under conditions of high moisture. Gliding motility was determined as described by Bowman (2000). Cell movement at colony edges was verified by using phase-contrast microscopy. Susceptibility to antibiotics was examined by the routine diffusion plate method. Discs 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) and tetracycline (30 µg).
The organisms isolated in this study were Gram-negative, chemo-organotrophic with respiratory-type metabolism, non-motile, single, flexible rods that were 0·4–0·5 µm in diameter and 2·5–7·3 µm in length. Optimal growth was observed at 1·5–2 % NaCl. Temperature range for growth was 4–34 °C for KMM 3912T and 4–36 °C for KMM 3976, with optimum growth occurring at 21–23 °C. pH range for growth was 5·5–10·0, with optimum growth occurring between pH 7·1 and 8·3. Both strains were susceptible to carbenicillin and lincomycin and strain KMM 3912T was also susceptible to oleandomycin and tetracycline. Other physiological and biochemical findings are listed in Table 1 and the species description.
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6c (1·2 %), i-C16 : 0 (2·8 %), i-C16 : 1 (4·2 %), C16 : 17/i-C15 : 0 2-OH (5·7 %), i-C17 : 19c (3·7 %), C17 : 16c (1·5 %), C15 : 0 2-OH (1·2 %), i-C15 : 0 3-OH (3·3 %), C15 : 0 3-OH (1·3 %), i-C16 : 0 3-OH (8·7 %), i-C17 : 0 3-OH (17·2 %), C17 : 0 2-OH (1·7 %) and unidentified fatty acids (3·2 %). The predominant fatty acids were straight- and branched-chain unsaturated, namely, i-C15 : 0, i-C15 : 1, i-C16 : 0 3-OH and i-C17 : 0 3-OH, which represented 59·7 % of the total fatty acids. It should be noted that the whole-cell fatty acid profile of strain KMM 3912T was characterized by the presence of 79·3 % branched fatty acids. These results are consistent with data reported for other representatives of the family Flavobacteriaceae (Bruns et al., 2001; Nedashkovskaya et al., 2003b). Isoprenoid quinones were extracted from lyophilized cells and analysed as described by Akagawa-Matsushita et al. (1992). Isoprenoid quinone composition was characterized by HPLC (Shimadzu), using a reverse-phase type Zorbax ODS column (250x4·6 mm) and acetonitrile/propan-2-ol (65 : 35, v/v) as the mobile phase at a flow rate of 0·5 ml min-1. The column was kept at 40 °C. Menaquinones were detected by monitoring A270 and were identified by comparison with known quinones from reference strain Salegentibacter salegens DSM 5424T. The main lipoquinone was MK-6.
DNA was isolated following the method of Marmur (1961) and its G+C content was determined by the thermal denaturation method (Marmur & Doty, 1962). DNA–DNA hybridization was performed spectrophotometrically and initial renaturation rates were recorded as described by De Ley et al. (1970). The DNA G+C content was 36·7–38·0 mol% as determined by the thermal denaturation method. DNA–DNA relatedness between KMM 3912T and KMM 3976 was 85 %.
DNA extraction, PCR and sequencing of 16S rDNA followed previous procedures (Kim et al., 1998). The obtained sequence data were aligned with those of representative members of selected genera of the family Flavobacteriaceae by using PHYDIT version 3.2 (http://plaza.snu.ac.kr/
jchun/phydit/). Phylogenetic trees were inferred by using suitable programs of the PHYLIP package (Felsenstein, 1993). Phylogenetic distances were calculated from the models of Kimura (1980) and trees were constructed on the basis of the neighbour-joining (Saitou & Nei, 1987), least-squares (Fitch & Margoliash, 1967) and maximum-likelihood (Felsenstein, 1993) algorithms. Bootstrap analysis was performed with 1000 resampled datasets by using the SEQBOOT and CONSENSE programs of the PHYLIP package.
Phylogenetic analysis of almost-complete 16S rDNA sequence (1385 nucleotide positions) revealed that strain KMM 3912T forms a distinct lineage in a cluster that includes members of the family Flavobacteriaceae (Bernardet et al., 2002), such as Cellulophaga, Arenibacter, Zobellia, Muricauda, Aequorivita, Vitellibacter and [Cytophaga] marinoflava (Fig. 1). 16S rDNA sequence similarity values of strain KMM 3912T to its closest relatives, Cellulophaga lytica, Cellulophaga fucicola and [Cytophaga] marinoflava, were 92·2, 92·1 and 91·7 %, respectively. The low sequence similarity levels of the strain tested to other members of the CFB phylum that have been described to date (86·2–91·5 %) clearly demonstrate that the bacteria isolated in this study represent a novel genus. Results of phenotypic analysis, including production of flexirubin pigments and inability to oxidize carbohydrates or hydrolyse starch, in combination with phylogenetic distinctiveness, allow the differentiation of strains KMM 3912T and KMM 3976 from their nearest neighbours, including Cellulophaga lytica, Cellulophaga fucicola and [Cytophaga] marinoflava. Phenotypic features that separate the strains studied from other members of the family Flavobacteriaceae are shown in Table 1
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Description of Ulvibacter gen. nov.
Ulvibacter (Ul.vi.bac'ter. N.L. fem. n. Ulva generic name of the green alga Ulva fenestrata; N.L. masc. n. bacter from Gr. n. bakterion rod; N.L. masc. n. Ulvibacter rod isolated from the green alga Ulva fenestrata).
Rod-shaped, non-motile cells. Gram-negative. Endospores are not formed. Na+ ions are required for growth. Strictly aerobic. Non-diffusible, yellow–orange pigments are produced. Flexirubins are formed. Chemo-organotrophic. Cytochrome oxidase-, catalase- and alkaline phosphatase-positive. Major respiratory quinone is MK-6. Main cellular fatty acids are the straight- and branched-chain unsaturated fatty acids i-C15 : 0, i-C15 : 1, i-C16 : 0 3-OH and i-C17 : 0 3-OH. As determined by 16S rDNA sequence analysis, the genus Ulvibacter is a member of the family Flavobacteriaceae within the phylum Cytophaga–Flavobacterium–Bacteroides. The type species is Ulvibacter litoralis.
Description of Ulvibacter litoralis sp. nov.
Ulvibacter litoralis (li.to.ra'lis. L. masc. adj. litoralis of the shore, a shallow-water dweller).
Main characteristics are as given for the genus. In addition, cells range from 0·4 to 0·5 µm in width and from 2·5 to 7·3 µm in length. On marine agar, colonies are 2–4 mm in diameter, circular, convex, shiny with entire edges, viscous and yellow–orange in colour. Growth is observed at 4–36 °C. Optimal temperature for growth is 21–23 °C. Growth occurs at 1–6 % NaCl. Gelatin, Tweens 20 and 40 and DNA are decomposed. Agar, casein, alginate, starch, Tween 80, cellulose (CM-cellulose and filter paper) and chitin are not hydrolysed. No acid is formed from cellobiose, fucose, galactose, melibiose, raffinose, rhamnose, xylose, adonitol, dulcitol or glycerol. Arabinose, glucose, lactose, mannose, maltose, sucrose, mannitol, inositol, sorbitol, malonate, citrate, N-acetylglucosamine, gluconate, caprate, adipate, malate and phenylacetate are not utilized. Nitrate is reduced. Production of indole, H2S and acetoin (Voges–Proskauer reaction) is negative. DNA G+C content is 36·7–38·0 mol%.
Type strain is KMM 3912T (=KCTC 12104T=CCUG 47093T). Reference strain is KMM 3976. Isolated from the green alga Ulva fenestrata.
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ACKNOWLEDGEMENTS |
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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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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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