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Int J Syst Evol Microbiol 55 (2005), 321-323; DOI  10.1099/ijs.0.63256-0
© 2005 International Union of Microbiological Societies

Gillisia mitskevichiae sp. nov., a novel bacterium of the family Flavobacteriaceae, isolated from sea water

Olga I. Nedashkovskaya1, Seung Bum Kim2,{dagger}, Kang Hyun Lee2, Valery V. Mikhailov1 and Kyung Sook Bae2

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 Resource Center, Korea Institute of Bioscience and Biotechnology, 52 Oun Dong, Yusong, Daejon 305-333, Republic of Korea

Correspondence
Olga I. Nedashkovskaya
olganedashkovska{at}piboc.dvo.ru
or
olganedashkovska{at}yahoo.com


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The taxonomic position of a novel marine, heterotrophic, aerobic, pigmented bacterium, non-motile by gliding, that was isolated from a sea-water sample collected in the Sea of Japan, was determined. 16S rRNA gene sequence analysis revealed that strain KMM 6034T is a member of the genus Gillisia. The phenotypic and chemotaxonomic data showed that the isolate represents a novel species of the genus Gillisia, for which the name Gillisia mitskevichiae sp. nov. is proposed. The type strain is KMM 6034T (=KCTC 12261T=NBRC 100590T=LMG 22575T).

Published online ahead of print on 20 August 2004 as DOI 10.1099/ijs.0.63256-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Gillisia mitskevichiae KMM 6034T is AY576655.

{dagger}Present address: Department of Microbiology, School of Bioscience and Biotechnology, Chungnam National University, Yusong, Daejon 305-764, Republic of Korea. Back


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The genus Gillisia accommodates Gram-negative, strictly aerobic, heterotrophic, yellow-pigmented bacteria that are non-motile by gliding and belong to the family Flavobacteriaceae (Van Trappen et al., 2004Go). The strains of the single species of this genus, Gillisia limnaea, were isolated from microbial mats from Lake Fryxell in the McMurdo Dry Valleys, Antarctica. The genus Gillisia forms a phylogenetic cluster with the genera Mesonia, Salegentibacter and Psychroflexus.

During June 2000, we isolated an unknown bacterium from a sea-water sample collected in Amursky Bay, Gulf of Peter the Great, Sea of Japan. A polyphasic taxonomic study of strain KMM 6034T, cultured on marine agar 2216 at 25 °C for 48 h, indicates that the isolate represents a novel species of the genus Gillisia, for which the name Gillisia mitskevichiae sp. nov. is proposed.

Genomic DNA extraction, PCR and sequencing of the 16S rRNA gene followed previous procedures (Kim et al., 1998Go). The sequence data obtained were aligned with those of members of the family Flavobacteriaceae 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, 1993Go). Phylogenetic distances were calculated from the model of Kimura (1980)Go and trees were constructed on the basis of the neighbour-joining (Saitou & Nei, 1987Go) and maximum-likelihood (Felsenstein, 1993Go) algorithms. Bootstrap analysis was performed with 1000 resampled datasets by using SEQBOOT and CONSENSE programs of the PHYLIP package.

Phylogenetic analysis of the almost-complete 16S rRNA gene sequence (1430 nucleotide positions) revealed that strain KMM 6034T was a member of the family Flavobacteriaceae and formed a distinct lineage within the genus Gillisia (Fig. 1Go). The level of 16S rRNA gene sequence similarity between strains KMM 6034T and G. limnaea LMG 21470T was 96·7 %. 16S rRNA gene sequence similarity values of the strain studied with the next closest relatives Mesonia algae KMM 3909T, [Cytophaga] latercula ATCC 23177T, Salegentibacter salegens DSM 5424T, Psychroflexus torquis ACAM 623T and Kordia algicida OT-1T were 91·4, 92·2, 93·1, 91·4 and 90·5 %, respectively.



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  		Fig. 1. Phylogenetic tree based on the 16S rRNA gene sequences of KMM 6034T and related members of the family Flavobacteriaceae. Asterisks indicate branches that were also recovered with the maximum-likelihood algorithm and numbers at nodes are levels of bootstrap support (%) from 1000 resampled datasets. Bar, 0·01 substitutions per nucleotide position.

 
DNA was isolated following the method of Marmur (1961)Go and the G+C content of the DNA was determined by the thermal denaturation method (Marmur & Doty, 1962Go). The DNA G+C content of KMM 6034T was 36·4 mol%.

Analysis of fatty acid methyl esters was carried out according to the standard protocol of the Microbial Identification System (Microbial ID). The cellular fatty acids comprising more than 1 % for strain KMM 6034T were straight- and branched-chain unsaturated and saturated fatty acids, namely i-14 : 0 (1·2 %), i-15 : 1 (11·8 %), a-15 : 1 (2·4 %), i-15 : 0 (7·5 %), a-15 : 0 (5·1 %), 15 : 0 (4·4 %), 15 : 1{omega}6c (1·9 %), i-16 : 1 (6 %), i-16 : 0 (9·3 %), i-15 : 0 3-OH (1·1 %), 15 : 0 2-OH (2·4 %), i-17 : 1{omega}9c (4 %), a-17 : 1{omega}9c (2·1 %), 17 : 1{omega}6c (4·7 %), i-16 : 0 3-OH (7·2 %), 16 : 0 3-OH (1·2 %), i-17 : 0 3-OH (6·7 %), 17 : 0 2-OH (3·8 %), and summed feature 3 (11·1 %), comprising i-15 : 0 2-OH and/or 16 : 1{omega}7c, which corresponds to the fatty acid composition of G. limnaea (Van Trappen et al., 2004Go). Both the strain studied and G. limnaea strains contained similar amounts of branched fatty acids (>65 % of total).

Phenotypic analysis was performed by using previously described methods (Nedashkovskaya et al., 2003aGo, bGo). Gliding motility was determined as described by Bowman (2000)Go.

The physiological, morphological and biochemical characteristics of strain KMM 6034T are listed in the species description and Table 1Go. The similarities in phenotypic characteristics support the inclusion of the strain studied in the genus Gillisia. However, strain KMM 6034T clearly differed from strains of G. limnaea by the NaCl requirement for growth, growth at 12 % NaCl, maximum growth temperature (31 °C), acid production from carbohydrates, utilization of mannitol and the ability to degrade casein, urea, DNA and Tweens 20 and 40 (Table 1Go).


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  		Table 1. Phenotypic characteristics that distinguish Gillisia mitskevichiae sp. nov. from G. limnaea

Data from Van Trappen et al. (2004)Go and this study. Strains of both species are Gram-negative and are positive for respiratory type of metabolism, oxidase, catalase and alkaline phosphatase activities, growth at 1–5 % NaCl and at 5–30 °C, hydrolysis of gelatin and Tween 80, utilization of glucose and sucrose and susceptibility to ampicillin, carbenicillin, lincomycin and oleandomycin. Strains of both species are negative for gliding motility, requirement for organic growth factors, flexirubin pigments, nitrate reduction, H2S, indole and acetoin production, degradation of agar, starch, cellulose (CM-cellulose, filter paper) and chitin, acid formation from arabinose, cellobiose, fucose, galactose, lactose, maltose, melibiose, raffinose, rhamnose, sorbose, xylose, inositol, mannitol, sorbitol, glycerol, adonitol, dulcitol and citrate, utilization of arabinose, lactose, mannose, inositol, sorbitol, malonate and citrate and susceptibility to gentamicin, kanamycin, neomycin and polymyxin B.

 
The above-mentioned phenotypic features (Table 1Go) in association with molecular differences presented in this paper allow the differentiation of strain KMM 6034T from G. limnaea. Thus, we propose that strain KMM 6034T be placed in the genus Gillisia as the type strain of Gillisia mitskevichiae sp. nov.

Description of Gillisia mitskevichiae sp. nov.
Gillisia mitskevichiae (mit.ske'vi.chi.ae. N.L. gen. n. mitskevichiae of Mitskevich, in honour of Irina N. Mitskevich, Russian marine microbiologist, for her contributions to the development of marine microbiology).

Cells are Gram-negative, strictly aerobic with respiratory metabolism, chemo-organotrophic, asporogenic rods, non-motile by gliding, 0·5–0·7 µm wide and 3–4 µm long. Oxidase-, catalase-, urease- and alkaline phosphatase-positive. Colonies are circular, convex, shiny with entire edges, 1–3 mm in diameter on marine agar 2216. Produces yellow non-diffusible pigments. No growth is observed without Na+; grows at 1–12 % NaCl. Flexirubin pigments are absent. Growth occurs at 4–31 °C. The pH range of growth is 5·5–10·0, with optimum growth occurring between pH 7·6 and 8·3. Casein, gelatin, DNA, urea and Tweens 40 and 80 are degraded; does not hydrolyse agar, starch, cellulose (CM-cellulose and filter paper), chitin or Tween 20. Forms acid from glucose, sucrose and N-acetylglucosamine, but not from arabinose, cellobiose, fucose, galactose, lactose, maltose, melibiose, raffinose, rhamnose, xylose, adonitol, dulcitol, glycerol, inositol or mannitol. Does not utilize arabinose, lactose, mannose, inositol, mannitol, sorbitol or citrate 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, oleandomycin, lincomycin, streptomycin and tetracycline; resistant to kanamycin, benzylpenicillin, neomycin, gentamicin and polymyxin B. The predominant cellular fatty acids are straight-chain unsaturated, branched-chain unsaturated and saturated, namely i-15 : 0 (7·5 %), a-15 : 0 (5·1 %), i-15 : 1 (11·8 %), i-16 : 1 (6 %), i-16 : 0 (9·3 %), i-16 : 0 3-OH (7·2 %), i-17 : 0 3-OH (6·7 %) and summed feature 3 (11·1 %), consisting of i-15 : 0 2-OH and/or 16 : 1{omega}7c (64·7 % of total). The G+C content of the DNA is 36·4 mol%.

The type strain is KMM 6034T (=KCTC 12261T=NBRC 100590T=LMG 22575T), isolated from sea-water collected in Amursky Bay, Gulf of Peter the Great, Sea of Japan.


   ACKNOWLEDGEMENTS
 
This research was supported by grants of the Federal Agency for Sciences and Innovations of the Ministry for Education and Sciences of the Russian Federation (no. 2-2.16), the Russian Foundation for Basic Research (no. 05-04-48211) and the Program of Fundamental Investigations of the Presidium of the Russian Academy of Sciences ‘Molecular and Cell Biology’. S. B. K., K. H. L. and K. S. B. are also grateful for support from the KRIBB Research Initiative Program.


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Bowman, J. P. (2000). Description of Cellulophaga algicola sp. nov., isolated from the surfaces of Antarctic algae, and reclassification of Cytophaga uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Cellulophaga uliginosa comb. nov. Int J Syst Evol Microbiol 50, 1861–1868.

Felsenstein, J. (1993). PHYLIP (phylogeny inference package), version 3.5c. Department of Genetics, University of Washington, Seattle, USA.

Kim, S. B., Falconer, C., Williams, E. & Goodfellow, M. (1998). Streptomyces thermocarboxydovorans sp. nov. and Streptomyces thermocarboxydus sp. nov., two moderately thermophilic carboxydotrophic species isolated from soil. Int J Syst Bacteriol 48, 59–68.[Abstract/Free Full Text]

Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111–120.[CrossRef][Medline]

Marmur, J. (1961). A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3, 208–218.

Marmur, J. & Doty, P. (1962). Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5, 109–118.[Medline]

Nedashkovskaya, O. I., Suzuki, M., Vysotskii, M. V. & Mikhailov, V. V. (2003a). Reichenbachia agariperforans gen. nov., sp. nov., a novel marine bacterium in the phylum Cytophaga–Flavobacterium–Bacteroides. Int J Syst Evol Microbiol 53, 81–85.[Abstract/Free Full Text]

Nedashkovskaya, O. I., Suzuki, M., Vysotskii, M. V. & Mikhailov, V. V. (2003b). Vitellibacter vladivostokensis gen. nov., sp. nov., a new member of the phylum Cytophaga–Flavobacterium–Bacteroides. Int J Syst Evol Microbiol 53, 1281–1286.[Abstract/Free Full Text]

Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.[Abstract]

Van Trappen, S., Vandecandelaere, I., Mergaert, J. & Swings, J. (2004). 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 54, 445–448.[Abstract/Free Full Text]




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