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Winogradskyella Thalassocola Gen. Nov., Sp. Nov., Winogradskyella Epiphytica Sp

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Winogradskyella Thalassocola Gen. Nov., Sp. Nov., Winogradskyella Epiphytica Sp International Journal of Systematic and Evolutionary Microbiology (2005), 55, 49–55 DOI 10.1099/ijs.0.63307-0 Winogradskyella thalassocola gen. nov., sp. nov., Winogradskyella epiphytica sp. nov. and Winogradskyella eximia sp. nov., marine bacteria of the family Flavobacteriaceae Olga I. Nedashkovskaya,1 Seung Bum Kim,23 Suk Kyun Han,2 Cindy Snauwaert,3 Marc Vancanneyt,3 Jean Swings,3,4 Kyung-Ok Kim,2 Anatoly M. Lysenko,5 Manfred Rohde,6 Galina M. Frolova,1 Valery V. Mikhailov1 and Kyung Sook Bae2 Correspondence 1Pacific Institute of Bioorganic Chemistry of the Far-Eastern Branch of the Russian Academy Olga I. Nedashkovskaya of Sciences, Pr. 100 let Vladivostoku 159, 690022, Vladivostok, Russia [email protected] 2Korean Collection for Type Cultures, Biological Resource Center, Korea Institute of or Bioscience and Biotechnology, Yusong, Daejon 305-333, Republic of Korea [email protected] 3,4BCCM/LMG Bacteria Collection3, and Laboratory of Microbiology4, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium 5Institute of Microbiology of the Russian Academy of Sciences, Pr. 60 let October 7/2, Moscow, 117811, Russia 6Bereich Mikrobiologie, Abt. Mikrobielle Pathogenitat und Impfstoffforschung, GBF – Gesellschaft fu¨r Biotechnologische Forschung, Mascheroder Weg 1, D-38124 Braunschweig, Germany Three novel heterotrophic, Gram-negative, yellow-pigmented, aerobic, gliding, oxidase- and catalase-positive bacteria were isolated from algae collected in the Gulf of Peter the Great, Sea of Japan. 16S rRNA gene sequence analysis revealed that the strains studied represented members of the family Flavobacteriaceae and showed 93?5–93?8 % similarity with their closest relative, Psychroserpens burtonensis. The DNA G+C content of the strains was 34–37 mol%. The major respiratory quinone was MK-6. The predominant fatty acids were iso-C15 : 0, anteiso-C15 : 0, iso-C15 : 1, iso-C16 : 0-3OH and iso-C17 : 0-3OH. On the basis of their phenotypic, chemotaxonomic, genotypic and phylogenetic characteristics, the newly described bacteria have been assigned to the new genus Winogradskyella gen. nov., as Winogradskyella thalassocola sp. nov. (type strain, KMM 3907T=KCTC 12221T=LMG 22492T=DSM 15363T), Winogradskyella epiphytica sp. nov. (type strain, KMM 3906T=KCTC 12220T=LMG 22491T=CCUG 47091T) and Winogradskyella eximia sp. nov. (type strain, KMM 3944T (=KCTC 12219T=LMG 22474T). Bacteria of the family Flavobacteriaceae are often found algicola, Formosa algae, Mesonia algae, Maribacter ulvicola, attached to the surfaces of a diverse range of marine algae Tenacibaculum amylolyticum, Ulvibacter litoralis and Zobellia (Chan & McManus, 1969; Bolinches et al., 1988; Hanzawa galactanivorans, associated with different algae, have been et al., 1998). The novel marine bacteria Arenibacter latericius, isolated and described (Johansen et al., 1999; Bowman, 2000; Cellulophaga fucicola, Cellulophaga baltica, Cellulophaga Barbeyron et al., 2001; Suzuki et al., 2001; Ivanova et al., 2001, 2004; Nedashkovskaya et al., 2003b, 2004a, b). The above- Published online ahead of print on 19 July 2004 as DOI 10.1099/ mentioned flavobacteria are commonly characterized by rod- ijs.0.63307-0. shaped cells. During studies on microbial communities of 3Present address: Department of Microbiology, School of Bioscience algae inhabiting the Sea of Japan, we recovered three novel and Biotechnology, Chungnam National University, Yusong, Daejon isolates belonging to the family Flavobacteriaceae from the 305-764, Republic of Korea. algae frond surfaces; these isolates were able to form cellular The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA network-like structures or aggregates that can be considered gene sequences of Winogradskyella thalassocola KMM 3907T, to serve for an attachment adaptation. Winogradskyella epiphytica KMM 3906T and Winogradskyella eximia KMM 3944T are AY521223, AY521224 and AY521225, respectively. Based on a polyphasic study of the algal isolates, including Downloaded from www.microbiologyresearch.org by 63307 G 2005 IUMS Printed in Great Britain 49 IP: 193.191.134.1 On: Fri, 21 Oct 2016 09:34:13 O. I. Nedashkovskaya and others phylogenetic, genotypic, chemotaxonomic and phenotypic The DNA G+C contents of strains KMM 3906T, KMM data, we propose a new genus, Winogradskyella gen. nov., 3907T and KMM 3944T were 35?2, 34?6 and 36?1 mol%, containing three novel species. respectively. DNA–DNA relatedness between the strains was T T T 34–45 %. These values indicated that the strains represent Strains KMM 3906 , KMM 3907 and KMM 3944 were three separate species. Phenotypic data distinguishing the isolated from the green alga Acrosiphonia sonderi, and the strains are given in Table 1. brown algae Chorda filum and Laminaria japonica, res- pectively, collected in the Gulf of Peter the Great of the Sea Analysis of fatty acid methyl esters was carried out of Japan during June 2000. Strains were cultivated at 28 uC according to the standard protocol of the Microbial on marine agar 2216 (MA; Difco) and stored at 280 uCin Identification System (Microbial ID). Isoprenoid quinones marine broth 2216 (MB; Difco) supplemented with 20 % were extracted from lyophilized cells and analysed as (v/v) glycerol. On MA, colonies of strains studied were described by Akagawa-Matsushita et al. (1992). Isoprenoid round, 2–4 mm in diameter, yellow-pigmented, shiny, quinone composition was characterized by HPLC viscous and with entire edges. (Shimadzu Instruments) using a reversed-phase type Zorbax ODS column (25064?6 mm) and acetonitrile/ The phylogenetic position of the three isolates was deter- 2-propanol (65 : 35, v/v) as a mobile phase at a flow rate mined using previously described procedures for DNA 21 of 0?5 ml min . The column was kept at 40 uC. extraction, PCR and 16S rRNA gene sequence analysis (Kim Menaquinones were detected by monitoring at 270 nm et al., 1998). The sequence data were aligned with those of and were identified by comparison with known quinones representative members of selected genera of the family T from reference strain Salegentibacter salegens DSM 5424 . Flavobacteriaceae by using PHYDIT version 3.2 (http:// plaza.snu.ac.kr/~jchun/phydit/). Phylogenetic trees were Predominant cellular fatty acids of the strains studied were inferred by using suitable programs of the PHYLIP package branched-chain unsaturated and straight-chain saturated, (Felsenstein, 1993). Phylogenetic distances were calculated namely iso-C15 : 0, anteiso-C15 : 0, iso-C15 : 1, iso-C16 : 0-3OH from the two-parameter model of Kimura (1980), and and iso-C17 : 0-3OH (Table 2). The major isoprenoid trees were constructed on the basis of the neighbour- quinone was MK-6. joining (Saitou & Nei, 1987), least-squares (Fitch & Margoliash, 1967) and maximum-likelihood (Felsenstein, Phenotypic characterization was performed using the 1993) algorithms. Bootstrap analysis was performed with tests described previously (Nedashkovskaya et al., 2003a, 1000 resampled datasets using the SEQBOOT and CONSENSE b). Gliding motility was determined as described by programs of the PHYLIP package. Bowman (2000). Scanning electron microscopy was used to examine the bacteria, which were fixed with a solution Phylogenetic analysis of almost-complete 16S rRNA gene containing 2 % glutaraldehyde and 3 % formaldehyde in T T sequences of strains KMM 3906 , KMM 3907 and KMM cacodylate buffer (0?1 M cacodylate, 0?09 M sucrose, 3944T revealed that they form a distinct lineage within the 0?01 M CaCl2,0?01 M MgCl2,pH6?9) for 1 h on ice and family Flavobacteriaceae (Fig. 1). Psychroserpens burtonensis washed with cacodylate buffer. After washing several times was found to be the nearest neighbour; this relationship in TE buffer (20 mM Tris, 1 mM EDTA, pH 7?0), samples was supported by a high bootstrap value and also by the were dehydrated through a graded series of acetone (10, 30, different tree-making algorithms used. However, 16S rRNA 50, 70, 90, 100 %) on ice, each step for 15 min, followed by gene sequence similarity between the three strains and P. critical-point drying with liquid CO2. Samples were sputter- burtonensis was only 93?5–93?8 %. 16S rRNA gene sequence coated with an approximately 10 nm thick gold film before similarity values of the three strains to other close relatives, examination in a Zeiss field-emission scanning electron Gelidibacter algens and Formosa algae, were 90?8–91?3 and microscope (DSM982 Gemini) at an acceleration voltage of 92?7–92?9 %, respectively. The low sequence similarity T T T 5 kV using the Everhart Thornley secondary electron (SE) values of KMM 3906 , KMM 3907 and KMM 3944 to detector and the Inlens-SE detector at a 50 : 50 ratio. other Cytophaga-like bacteria described to date (85?6– 92?1 %) demonstrate that the bacteria isolated in this The three bacteria described in this study were Gram- study represent a new genus. negative, chemo-organotrophic with respiratory-type meta- bolism, non-motile single flexible rods, 0?4–0?6 mmin The three strains had 16S rRNA gene sequence similarities ? ? m in the range 96?3–97?1%. diameter and 1 0–1 3 m in length. All three strains formed unique network-like structures or aggregates (Fig. 2A–C). For DNA–DNA hybridizations and determination of the Growth of strain KMM 3944T was observed at 1–5 % NaCl; G+C content, DNA was isolated following the method of strains KMM 3906T and KMM 3907T grew in media Marmur (1961). The G+C content was determined by the containing 1–8 % NaCl. Optimal growth was observed at thermal denaturation method of Marmur & Doty (1962). 1?5–2 % NaCl. The maximum growth temperature for strain DNA–DNA hybridization was performed spectrophoto- KMM 3906T was 37 uC, and that for strains KMM 3907T and metrically and initial renaturation rates were recorded as KMM 3944T was 33 uC. Strain KMM 3906T was able to described by De Ley et al. (1970). oxidize carbohydrates, but the other two strains were not. Downloaded from www.microbiologyresearch.org by 50 International Journal of Systematic and Evolutionary Microbiology 55 IP: 193.191.134.1 On: Fri, 21 Oct 2016 09:34:13 Winogradskyella gen.
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