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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 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
Correspondence
Olga I. Nedashkovskaya
olganedashkovska{at}yahoo.com
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ABSTRACT |
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-galactosidase- and alkaline phosphatase-positive. 16S rRNA gene sequence phylogenetic analysis indicated that the strains KMM 6020T, KMM 6021 and KMM 6028 occupied a distinct lineage within the family Flavobacteriaceae. The major respiratory quinone was MK-6. The predominant fatty acids were i15 : 0, i15 : 1, i15 : 0 3-OH, i17 : 1
9c and i17 : 0 3-OH. On the basis of phenotypic, chemotaxonomic, genotypic and phylogenetic characteristics, the novel bacteria were assigned to the genus Aquimarina gen. nov., as Aquimarina muelleri gen. nov., sp. nov. The type strain is KMM 6020T (=KCTC 12285T=LMG 22569T). From the results of the 16S rRNA gene sequence analysis and phenotypic features, the species [Cytophaga] latercula Lewin 1969
is proposed to be reclassified in the new genus Stanierella as Stanierella latercula gen. nov., comb. nov., with type strain CIP 104806T (=ATCC 23177T=NCIMB 1399T=LMG 1343T).
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Aquimarina muelleri KMM 6020T, KMM 6021 and KMM 6028 are AY608406, AY608407 and AY608408, respectively.
Present address: Department of Microbiology, School of Bioscience and Biotechnology, Chungnam National University, Yusong, Daejon 305-764, Republic of Korea. 
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to accommodate Gram-negative, motile by gliding, aerobic, pigmented and cellulolytic bacteria. Many other novel bacteria were later included in the genus Cytophaga, which was consequently emended by Reichenbach (1989) and Nakagawa & Yamasato (1996). The latter authors proposed to restrict the polyphyletic genus Cytophaga to the species Cytophaga aurantiaca and Cytophaga hutchinsonii according to phylogenetic analysis data based on 16S rRNA gene sequence analysis. Novel genera were proposed for some Cytophaga species. For example, [Cytophaga] agarovorans Reichenbach 1989 and [Cytophaga] salmonicolor Veldkamp 1961 were reclassified as Marinilabilia agarovorans and Marinilabilia salmonicolor, respectively, by Nakagawa & Yamasato (1996). These species were subsequently merged into a single species M. salmonicolor on the basis of DNA–DNA hybridization experiments (Suzuki et al., 1999). The novel genera Flammeovirga and Persicobacter were created, based on determination of their precise phylogenetic positions and polyamine compositions by Nakagawa et al. (1997), to accommodate [Cytophaga] aprica Reichenbach 1989 and [Cytophaga] diffluens Reichenbach 1989, respectively. Several Cytophaga species, [Cytophaga] aquatilis Strohl and Tait 1978, [Cytophaga] columnaris Bernardet and Grimont 1989, [Cytophaga] flevense van der Meulen et al. 1974, [Cytophaga] johnsoniae Stanier 1947, [Cytophaga] pectinivora Reichenbach 1989, [Cytophaga] psychrophila Reichenbach 1989, [Cytophaga] saccharophila Reichenbach 1989 and [Cytophaga] succinicans Reichenbach 1989, were transferred to the genus Flavobacterium (Bernardet et al., 1996). [Cytophaga] heparina Christensen 1980 was reclassified as Sphingobacterium heparinum Takeuchi and Yokota 1993 (effective publication by Takeuchi & Yokota, 1992), and later transferred to the genus Pedobacter as Pedobacter heparinum (Steyn et al., 1998). The marine bacteria [Cytophaga] lytica Lewin 1969 and [Cytophaga] marina Reichenbach 1989 were included in the new genera Cellulophaga (Johansen et al., 1999) and Tenacibaculum (Suzuki et al., 2001), respectively, as the type species of these taxa. A marine bacterium isolated from a mud sample and described as [Flavobacterium] uliginosum (ZoBell & Upham, 1944) is now included in the genus Zobellia (Barbeyron et al., 2001). Currently, only two of the 20 species initially included in the genus Cytophaga by Reichenbach (1989), [Cytophaga] latercula and [Cytophaga] marinoflava, together with [Cytophaga] fermentans Bachmann 1955, [Cytophaga] arvensicola Oyaizu et al. 1983 (effective publication by Oyaizu et al., 1982) and [Cytophaga] xylanolytica Haak and Breznak 1993, are considered as misnamed Cytophaga species and remain to be reclassified.
In the course of a study of a sea-water microbial population, novel heterotrophic, aerobic, Gram-negative, gliding and flexirubin-producing bacteria were isolated. 16S rRNA gene sequence analysis indicated that the isolates were members of the family Flavobacteriaceae, in which they form a distinct lineage. The closest relative of the strains studied was [Cytophaga] latercula (95·4 % sequence similarity). However, based on differences in the molecular and phenotypic features described here, we proposed that the KMM strains clearly differ from strain [Cytophaga] latercula CIP 104806T and represent a separate genus of the family Flavobacteriaceae. Consequently, we propose the description of the novel genus and species Aquimarina muelleri gen. nov., sp. nov., with type strain KMM 6020T, and the reclassification of [Cytophaga] latercula Lewin 1969 in the new genus Stanierella as Stanierella latercula gen. nov., comb. nov., with type strain CIP 104806T.
Strains KMM 6020T, KMM 6021 and KMM 6028 were isolated from a sea-water sample collected in Amursky Bay, Gulf of Peter the Great, Sea of Japan. After primary isolation and purification on marine agar, strains were cultivated at 28 °C on the same medium and stored at –80 °C in marine broth supplemented with 20 % (v/v) glycerol.
Genomic DNA extraction, PCR and sequencing of the 16S rRNA gene followed the procedures of Kim et al. (1998). The sequence data obtained were aligned together with those of representative members of the family Flavobacteriaceae by PHYDIT version 3.2 (http://plaza.snu.ac.kr/
jchun/phydit/). Phylogenetic trees were inferred using suitable programs of the PHYLIP package (Felsenstein, 1993). Phylogenetic distances were calculated from the models of Kimura (1980), and phylogenetic trees were constructed on the basis of the neighbour-joining (Saitou & Nei, 1987) and maximum-likelihood (Felsenstein, 1993) algorithms. Bootstrap analysis was performed with 1000 resamplings, using the SEQBOOT and CONSENSE programs of the PHYLIP package.
Phylogenetic 16S rRNA gene sequence analysis indicated that strains KMM 6020T, KMM 6021 and KMM 6028 are members of the family Flavobacteriaceae and form a cluster with species of the genera Psychroflexus, Salegentibacter and Mesonia (Fig. 1). The closest relative of these strains is [Cytophaga] latercula CIP 104806T, with 95·4 % sequence similarity.
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and G+C content was determined by the thermal denaturation method of Marmur & Doty (1962). The G+C content of the DNA of the strains studied ranges from 31·6 to 32·5 mol%. DNA–DNA hybridizations were performed spectrophotometrically and initial renaturation rates were recorded as described by De Ley et al. (1970). The level of DNA–DNA relatedness between the KMM strains was 85–99 %. These values are significantly more than 70 %, and therefore suggest that the strains belong to the same species (Wayne et al., 1987).
Analysis of fatty acid methyl esters was carried out according to the standard protocol of the Microbial Identification System (Microbial ID). The major cellular fatty acids of the sea-water isolates were i15 : 1, i15 : 0, i15 : 0 3-OH, i17 : 19c and i17 : 0 3-OH (9·8–13, 19·3–21·1, 5·5–7·5, 9·3–10·6 and 21–29·5 %, respectively), and summed feature 3 (7–8·4 %), comprising 16 : 17 and/or i15 : 0 2-OH fatty acids. Isoprenoid quinones were extracted from lyophilized cells and analysed as described by Nedashkovskaya et al. (2003c); the major respiratory quinone was MK-6.
Phenotypic analysis was performed using the methods of Nedashkovskaya et al. (2003a, b). Gliding motility was determined as described by Bowman (2000).
Physiological, biochemical and morphological characteristics of the strains studied are listed under the species description and are also given in Table 1. Phenotypic examination demonstrated many common traits between the strains studied and [Cytophaga] latercula. However, the KMM strains differ sufficiently from their closest relative on the basis of the ability to move by gliding motility, catalase activity, hydrolysis of agar and starch, flexirubin pigments and hydrogen sulphide production. Differential characteristics of the strains studied and their nearest relatives are shown in Table 1.
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Description of Aquimarina gen. nov.
Aquimarina (A.qui.ma.ri'na. L. fem. n. aqua water; L. adj. marinus, -a, -um marine; N.L. adj. aquimarina living in sea water).
Rod-shaped cells, motile by gliding. Gram-negative. Do not form endospores. Strictly aerobic. Produce non-diffusible yellow pigments. Chemo-organotroph. Cytochrome oxidase-, catalase- and alkaline phosphatase-positive. The predominant cellular fatty acids are straight-chain saturated, branched-chain saturated and unsaturated fatty acids: i15 : 0, i15 : 1, i15 : 0 3-OH, i17 : 19c, i17 : 0 3-OH and summed feature 3 (comprising 16 : 17c and/or i15 : 0 2-OH fatty acids). The main lipoquinone is MK-6. 16S rRNA gene sequence analysis indicates the genus Aquimarina is a member of the family Flavobacteriaceae, phylum ‘Bacteroidetes’. The type species is Aquimarina muelleri.
Description of Aquimarina muelleri sp. nov.
Aquimarina muelleri [muel'le.ri. N.L. gen. n. muelleri of Müller, in honour of Otto Friedrich Müller (1730–1784), the famous Danish naturalist, for his contributions to the development of marine microbiology].
Characteristics are as given for the genus. In addition, cells are 0·3–0·5 µm in width and 5–7 µm in length. Colonies are irregularly shaped, flat, with non-entire edges and 3–5 mm in diameter on marine agar 2216. Produces dark yellow to brown non-diffusible pigments. No growth is observed without Na+. Growth occurs at 1–8 % NaCl. Flexirubin pigments are formed. Growth occurs at 4–34 °C. Casein, gelatin, starch, DNA and Tweens 20, 40, 60 and 80 are degraded. Does not hydrolyse agar, alginate, urea, chitin or cellulose (CM-cellulose or filter paper). Does not form acid from arabinose, cellobiose, fucose, galactose, glucose, lactose, maltose, melibiose, raffinose, rhamnose, sucrose, xylose, adonitol, dulcitol, glycerol, inositol, mannitol or N-acetylglucosamine. Does not utilize arabinose, glucose, lactose, mannose, sucrose, inositol, mannitol, sorbitol, citrate or malonate as sole sources of carbon and energy. Nitrate reduction is negative. H2S, indole and acetoin (Voges–Proskauer reaction) are not produced. Susceptible to ampicillin, carbenicillin, lincomycin and oleandomycin. Resistant to benzylpenicillin, gentamicin, kanamycin, neomycin and polymyxin B. The predominant cellular fatty acids are straight-chain unsaturated, branched-chain unsaturated and saturated: i15 : 0 (19·3–21·1 %), i15 : 1 (9·8–13 %), i15 : 0 3-OH (5·5–7·5 %), i17 : 19c (9·3–10·6 %), i17 : 0 3-OH (21–29·5 %) and summed feature 3 (7–8·4 %; comprising i15 : 0 2-OH and/or 16 : 17c fatty acids). G+C content of the DNA is 31·6–32·5 mol%.
The type strain, KMM 6020T (=KCTC 12285T=LMG 22569T), was isolated from a sea-water sample collected in Amursky Bay, Gulf of Peter the Great, Sea of Japan.
Description of Stanierella gen. nov.
Stanierella [Sta'ni.er.el.la. L. dim. ending -ella; N.L. fem. n. Stanierella named in honour of the famous Canadian microbiologist Roger Y. Stanier (1916–1982), for his important contributions to the development of marine microbiology and the taxonomy of the Cytophaga-like bacteria].
Rod-shaped cells, non-motile. Gram-negative. Do not form endospores. Strictly aerobic. Produces non-diffusible pigments. No flexirubins are formed. Chemo-organotroph. Cytochrome oxidase- and alkaline phosphatase-positive; catalase-negative. The main lipoquinone is MK-6. 16S rRNA gene sequence analysis indicates the genus Stanierella is a member of the family Flavobacteriaceae, phylum ‘Bacteroidetes’. The type species is Stanierella latercula.
Description of Stanierella latercula comb. nov.
Stanierella latercula (la.ter'cu.la. L. masc. n. laterculus a small brick; N.L. fem. adj. latercula brick-like, brick-red colour).
Basonym: Cytophaga latercula Lewin 1969.
The description is as given for the genus and by Reichenbach (1989), with the addition that it is -galactosidase-positive. Degrades casein, DNA and Tweens 20, 40 and 80, but not urea or cellulose (CM-cellulose or filter paper). Does not form acid from L-arabinose, D-cellobiose, L-fucose, D-galactose, D-glucose, D-lactose, D-maltose, D-melibiose, L-raffinose, L-rhamnose, D-sucrose, DL-xylose, adonitol, dulcitol, glycerol, inositol, mannitol or N-acetylglucosamine. Growth occurs at 4–34 °C and at 1–5 % NaCl. Susceptible to ampicillin, lincomycin, oleandomycin and streptomycin. Resistant to benzylpenicillin, carbenicillin, gentamicin, kanamycin, neomycin and polymyxin B. The predominant cellular fatty acids are straight-chain saturated, branched-chain saturated and unsaturated fatty acids: i15 : 0 (18·2 %), i15 : 1w10c (6·7 %), 15 : 0 (5·4 %), i15 : 0 3-OH (7·1 %), i17 : 17c (11·6 %) and i17 : 0 3-OH (34·7 %) (Bowman et al., 1998). G+C content of the DNA is 34 mol%.
The type strain, CIP 104806T (=ATCC 23177T=NCIMB 1399T=LMG 1343T), was isolated from the outflow of a marine aquarium in La Jolla, CA, USA.
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ACKNOWLEDGEMENTS |
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O. I. Nedashkovskaya, M. Vancanneyt, P. Dawyndt, K. Engelbeen, K. Vandemeulebroecke, I. Cleenwerck, B. Hoste, J. Mergaert, T.-L. Tan, G. M. Frolova, et al. Reclassification of [Cytophaga] marinoflava Reichenbach 1989 as Leeuwenhoekiella marinoflava gen. nov., comb. nov. and description of Leeuwenhoekiella aequorea sp. nov. Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1033 - 1038. [Abstract] [Full Text] [PDF]
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