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Int J Syst Evol Microbiol 55 (2005), 235-238; DOI  10.1099/ijs.0.63297-0
© 2005 International Union of Microbiological Societies

Salegentibacter mishustinae sp. nov., isolated from the sea urchin Strongylocentrotus intermedius

Olga I. Nedashkovskaya1, Seung Bum Kim2,{dagger}, Anatoly M. Lysenko3, Valery V. Mikhailov1, Kyung Sook Bae2 and In Seop Kim4

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, 52 Oun-Dong, 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 Department of Biological Sciences, Hannam University, 133 Ojung Dong, Daeduk, Daejon 306-791, Republic of Korea

Correspondence
Olga I. Nedashkovskaya
olganedashkovska{at}yahoo.com


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A bacterial strain, designated KMM 6049T, was isolated from the sea urchin Strongylocentrotus intermedius inhabiting the Sea of Japan. The bacterium studied was strictly aerobic, heterotrophic, yellow-pigmented, non-motile, Gram-negative and oxidase-, catalase-, {beta}-galactosidase- and alkaline phosphatase-positive. 16S rRNA gene sequence analysis indicated that strain KMM 3524T was closely related to Salegentibacter holothuriorum and Salegentibacter salegens (sharing 97·7 and 98 % sequence similarity, respectively). DNA–DNA relatedness levels between strains KMM 6049T and S. holothuriorum KMM 3524T and S. salegens DSM 5424T were 24 and 45 %, respectively, indicating that KMM 6049T belongs to a novel species of the genus Salegentibacter, for which the name Salegentibacter mishustinae sp. nov. is proposed. The type strain is KMM 6049T (=KCTC 12263T=LMG 22584T=NBRC 100592T).

Published online ahead of print on 6 August 2004 as DOI 10.1099/ijs.0.63297-0.

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Salegentibacter mishustinae KMM 6049T is AY576653.

{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 Salegentibacter was created by McCammon & Bowman (2000)Go to accommodate moderately halophilic, yellow-pigmented bacteria that are not motile by gliding. This genus comprises two recognized species: Salegentibacter salegens, formerly Flavobacterium salegens (Dobson et al., 1993Go), isolated from a hypersaline meromictic lake in Antarctica, and Salegentibacter holothuriorum, recovered from the edible holothurian Apostichopus japonicus in the Sea of Japan (McCammon & Bowman, 2000Go; Nedashkovskaya et al., 2004Go).

In the course of our study of the microbial community associated with the sea urchin Strongylocentrotus intermedius, which is common in the Sea of Japan, an unknown marine bacterium was isolated, designated strain KMM 6049T. 16S rRNA gene sequence analysis revealed that strain KMM 6049T falls within the genus Salegentibacter. DNA–DNA hybridization data clearly indicated that the isolate represents a novel species of the genus Salegentibacter, for which the name Salegentibacter mishustinae sp. nov. is proposed.

Strain KMM 6049T was isolated from the sea urchin Strongylocentrotus intermedius collected in Troitsa Bay, Gulf of Peter the Great, Sea of Japan, in September 2002 from a water depth of 3 m. For isolation, 0·1 ml tissue homogenates was transferred to marine agar plates. After primary isolation and purification, isolates 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 16S rRNA gene sequencing followed the procedures of Kim et al. (1998)Go. The sequence data obtained were aligned with those of representative members of selected genera belonging to the family Flavobacteriaceae using PHYDIT version 3.2 (http://plaza.snu.ac.kr/~jchun/phydit/). Phylogenetic trees were inferred using suitable programs of the PHYLIP package (Felsenstein, 1993Go). Phylogenetic distances were calculated from the models 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 resamplings using the SEQBOOT and CONSENSE programs of the PHYLIP package.

16S rRNA gene sequence analysis indicated that strain KMM 6049T is a member of the genus Salegentibacter with closest relative S. holothuriorum KMM 3524T (Fig. 1Go). 16S rRNA gene sequence similarities between strain KMM 6049T and S. holothuriorum KMM 3524T and S. salegens DSM 5424T are 98 and 97·7 %, respectively.



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  		Fig. 1. Phylogenetic tree based on the 16S rRNA gene sequences of strain KMM 6049T and related members of the family Flavobacteriaceae. Asterisks indicate branches that were also recovered in the maximum-likelihood algorithm, and numbers at nodes are levels of bootstrap support (%) from 1000 resamplings. Bar, 0·01 substitutions per nucleotide position.

 
DNA was isolated following the method of Marmur (1961)Go and the G+C content was determined by the thermal denaturation method of Marmur & Doty (1962)Go. The DNA G+C content of strain KMM 6049T was 37·5 mol%. DNA–DNA hybridization experiments were performed using the method of De Ley et al. (1970)Go. DNA–DNA relatedness levels between strain KMM 6049T and S. salegens DSM 5424T and S. holothuriorum were 45 and 24 %, respectively. The DNA hybridization results show that the strain studied belongs to a novel species of the genus Salegentibacter (Wayne et al., 1987Go).

Analysis of fatty acid methyl esters was carried out according to the standard protocol of the Microbial Identification System (Microbial ID). The main cellular fatty acids were i15 : 1 (12·3 %), i15 : 0 (7·5 %), a15 : 0 (7·9 %), 15 : 0 (6·7 %), i17 : 0 3-OH (8·6 %) and summed feature 3 (7·9 %), comprising 16 : 1{omega}7 and i15 : 0 2-OH fatty acids.

Flexirubin pigments were examined using the method of Fautz & Reichenbach (1980)Go. Oxidative or fermentative utilization of glucose was determined on Hugh & Leifson medium modified for marine bacteria (Lemos et al., 1985Go). The methods of Gerhardt et al. (1994)Go were used to test the following: Gram-staining reaction; degradation of starch, casein, gelatin, cellulose, chitin, DNA, urea and alginic acids; oxidase-, catalase-, {beta}-galactosidase- and alkaline phosphatase activities; growth at different temperatures, NaCl concentrations and pH; and production of acid from carbohydrates. Utilization of carbon sources, spreading growth and temperature range for growth were examined as described by Nedashkovskaya et al. (2003b)Go. Susceptibility to antibiotics was tested as described by Nedashkovskaya et al. (2003a)Go. Gliding motility was determined as described by Bowman (2000)Go.

The physiological, biochemical and morphological characteristics of strain KMM 6049T are given under the species description and in Table 1Go. The phenotypic features of strain KMM 6049T are consistent with those of S. salegens and S. holothuriorum (Table 1Go). However, the strain studied differs from S. holothuriorum KMM 3524T in its ability to grow at 18 % NaCl, to decompose casein and to form acid from D-sucrose and L-raffinose and its resistance to carbenicillin. Strain KMM 6049T differs from S. salegens in its inability to reduce nitrate to nitrite, to hydrolyse DNA and to form acid from D-galactose and D-glucose and the absence of susceptibility to carbenicillin and streptomycin.


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  		Table 1. Phenotypic characteristics of strain KMM 6049T and Salegentibacter species

Species: 1, S. mishustinae sp. nov. KMM 6049T; 2, S. salegens; 3, S. holothuriorum KMM 3524T. Data from Dobson et al. (1993)Go, McCammon & Bowman (2000)Go, Nedashkovskaya et al. (2004)Go and this study. All strains were positive for the following tests: respiratory metabolism; oxidase, catalase, {beta}-galactosidase and alkaline phosphatase activities; hydrolysis of Tweens 20, 40 and 80, gelatin, elastin, starch and alginic acid; growth at 34 °C and 8 % NaCl; acid formation from D-maltose; utilization of D-glucose and D-mannose; H2S production; susceptibility to ampicillin, benzylpenicillin, lincomycin, oleandomycin and tetracycline; resistance to gentamicin, kanamycin, neomycin and polymyxin B. All strains were negative for: motility by gliding; hydrolysis of agar, cellulose (CM-cellulose and filter paper), urea and chitin; acid from L-arabinose, D-cellobiose, D-melibiose, L-rhamnose, L-sorbose, DL-xylose, succinate, citrate, glycerol, adonitol, dulcitol, sorbitol, inositol and mannitol; utilization of L-arabinose, inositol, mannitol, sorbitol, malonate and citrate; indole and acetoin (Voges–Proskauer reaction) production.

 
A combination of genomic distinctiveness and phenotypic and chemotaxonomic data allows us to classify strain KMM 6049T within the genus Salegentibacter, as a novel species, for which the name Salegentibacter mishustinae sp. nov. is proposed.

Description of Salegentibacter mishustinae sp. nov.
Salegentibacter mishustinae (mi.shu'sti.nae. N.L. gen. n. mishustinae of Mishustina, in honour of Irina E. Mishustina, Russian microbiologist, for her contributions to the development of marine microbiology).

Cells are Gram-negative, strictly aerobic, chemo-organotrophic, non-motile, asporogenic rods, 0·5–0·7 µm wide and 2·5–5·1 µm long. Oxidase-, catalase-, {beta}-galactosidase 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+. Growth occurs at 1–18 % NaCl. Flexirubin pigments are absent. Growth is detected at 4 and 36 °C. Hydrolyses gelatin, casein, elastin, starch, alginic acids and Tweens 20, 40 and 80, but not agar, DNA, cellulose (CM-cellulose and filter paper), chitin or urea. Forms acid from D-maltose, L-raffinose and D-sucrose, but not from L-arabinose, D-cellobiose, L-fucose, D-galactose, D-glucose, D-lactose, D-melibiose, L-rhamnose, L-sorbose, DL-xylose, adonitol, dulcitol, glycerol, inositol, sorbitol, mannitol or N-acetylglucosamine. Utilizes D-glucose, D-lactose, D-sucrose and D-mannose, but not L-arabinose, inositol, sorbitol, mannitol, citrate or malonate. H2S is produced. Nitrate reduction is negative. Produces no indole or acetoin (Voges–Proskauer reaction). Susceptible to ampicillin, benzylpenicillin, oleandomycin, lincomycin and tetracycline. Resistant to carbenicillin, kanamycin, neomycin, streptomycin, gentamicin and polymyxin B. The predominant cellular fatty acids are i15 : 1 (12·3 %), i15 : 0 (7·5 %), a15 : 0 (7·9 %), 15 : 0 (6·7 %), i17 : 0 3-OH (8·6 %) and summed feature 3 (7·9 %), comprising 16 : 1{omega}7 and i15 : 0 2-OH fatty acids. The DNA G+C content is 37·5 mol%.

The type strain, KMM 6049T (=KCTC 12263T=LMG 22584T=NBRC 100592T), was isolated from the sea urchin Strongylocentrotus intermedius, collected in Troitsa 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, Russian Foundation for Basic Research no. 05-04-48211 and Program of Fundamental Investigations of the Presidium of the Russian Academy of Sciences ‘Molecular and Cell Biology’. S. B. K. and K. S. B. acknowledge support from the KRIBB Research Initiative Program.


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De Ley, J., Cattoir, H. & Reynaerts, A. (1970). The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12, 133–142.[Medline]

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Fautz, E. & Reichenbach, H. (1980). A simple test for flexirubin-type pigments. FEMS Microbiol Lett 8, 87–91.

Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package), version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, USA.

Gerhardt, R., Murray, R. G. E., Wood, W. A. & Krieg, N. R. (editors) (1994). Methods for General and Molecular Bacteriology. Washington, DC: American Society for Microbiology.

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]

Lemos, M. L., Toranzo, A. E. & Barja, J. L. (1985). Modified medium for oxidation-fermentation test in the identification of marine bacteria. Appl Environ Microbiol 40, 1541–1543.

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]

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