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Int J Syst Evol Microbiol 56 (2006), 883-887; DOI  10.1099/ijs.0.64167-0
© 2006 International Union of Microbiological Societies

Salegentibacter agarivorans sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the sponge Artemisina sp.

Olga I. Nedashkovskaya1, Seung Bum Kim2, Marc Vancanneyt3, Dong Sung Shin2, Anatoly M. Lysenko4, Lyudmila S. Shevchenko1, Vladimir B. Krasokhin1, Valery V. Mikhailov1, Jean Swings3 and Kyung Sook Bae5

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 Department of Microbiology, School of Bioscience and Biotechnology, Chungnam National University, 220 Gung-dong, Yusong, Daejon 305-764, Republic of Korea
3 BCCM/LMG Bacteria Collection, Laboratory of Microbiology, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium
4 Institute of Microbiology of the Russian Academy of Sciences, Pr. 60 Let October 7/2, Moscow, 117811, Russia
5 Korea Research Institute of Bioscience and Biotechnology, 52 Oun-Dong, Yusong, Daejon 305-333, Republic of Korea

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


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A sponge-associated strain, KMM 7019T, was investigated in a polyphasic taxonomic study. The bacterium was strictly aerobic, heterotrophic, Gram-negative, yellow-pigmented, motile by gliding and oxidase-, catalase-, beta-galactosidase- and alkaline phosphatase-positive. A phylogenetic analysis based on 16S rRNA gene sequences revealed that strain KMM 7019T is closely related to members of the genus Salegentibacter, namely Salegentibacter holothuriorum, Salegentibacter mishustinae and Salegentibacter salegens (97·7–98 % sequence similarities). The DNA–DNA relatedness between the strain studied and Salegentibacter species ranged from 27 to 31 %, clearly demonstrating that KMM 7019T belongs to a novel species of the genus Salegentibacter, for which the name Salegentibacter agarivorans sp. nov. is proposed. The type strain is KMM 7019T (=KCTC 12560T=LMG 23205T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain KMM 7019T is DQ191176.


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Bacteria belonging to the genus Salegentibacter, a member of the family Flavobacteriaceae, are aerobic, halotolerant or halophilic, pigmented yellow or yellow–orange and motile by gliding (McCammon & Bowman, 2000Go). At present, there are three Salegentibacter species with validly published names: Salegentibacter salegens, formerly Flavobacterium salegens (Dobson et al., 1993Go), isolated from a meromictic lake in Antarctica; Salegentibacter holothuriorum, recovered from the edible holothurian Apostichopus japonicus in the Sea of Japan; and Salegentibacter mishustinae, isolated from the sea urchin Strongylocentrotus intermedius (McCammon & Bowman, 2000Go; Nedashkovskaya et al., 2004Go, 2005Go). The genus Mesonia is the nearest phylogenetic neighbour of Salegentibacter species.

During the 29th cruise of the R/V Akademician Oparin, a novel agar-decomposing bacterium, strain KMM 7019T, was isolated from a sponge (Artemisina sp.) collected in July 2003 near Onecotan Island, Kuril Islands, Sea of Okhotsk, Pacific Ocean, from a depth of 150 m. For strain isolation, 0·1 ml tissue homogenate was transferred to marine agar (Difco) plates. After primary isolation and purification the strain was cultivated at 28 °C on the same medium and stored at –80 °C in marine broth (Difco) supplemented with 20 % (v/v) glycerol.

Genomic DNA extraction, PCRs and sequencing of the 16S rRNA gene were performed according to published procedures (Kim et al., 1998Go). The sequence obtained was aligned, using PHYDIT, version 3.2 (http://plaza.snu.ac.kr/~jchun/phydit/), with those of representative members of selected genera belonging to the family Flavobacteriaceae. Phylogenetic trees were inferred by 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 resampled datasets by using the SEQBOOT and CONSENSE programs of the PHYLIP package.

Analysis of 16S rRNA gene sequences indicated that strain KMM 7019T is a member of the family Flavobacteriaceae and that its nearest neighbours are Salegentibacter holothuriorum KMM 3524T, Salegentibacter mishustinae KMM 6049T and Salegentibacter salegens DSM 5424T, with sequence similarities of 97·7–98·0 % (Fig. 1Go).


Figure 1
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  		Fig. 1. Phylogenetic tree based on the 16S rRNA gene sequences of KMM 7019T and related members of the family Flavobacteriaceae. Asterisks indicate branches that were also recovered in the maximum-likelihood algorithm. Numbers at nodes indicate levels of bootstrap support (%) from 1000 resamplings. Bar, 0·01 substitutions per nucleotide position.

 
DNA was isolated by following the method of Marmur (1961)Go, and the G+C content was determined by using the thermal denaturation method (Marmur & Doty, 1962Go). The DNA G+C content of the strain studied was 39·2 mol%. DNA–DNA hybridization experiments were performed using the method described by De Ley et al. (1970)Go. DNA–DNA relatedness levels between strain KMM 7019T and Salegentibacter species were in the range 27–31 %. These values are significantly below 70 %, and, consequently, the strain studied represents 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). All strains tested were grown on marine agar at 25 °C for 48 h. The predominant cellular fatty acids were C15 : 1 iso (12·1 %), C15 : 0 iso (12·3 %), C15 : 0 anteiso (7·1 %), C15 : 0 (5·6 %), C17 : 0 iso 3-OH (9·8 %) and summed feature 3 (12·2 %), comprising C16 : 1{omega}7c and/or C15 : 0 iso 2-OH. The complete fatty acid content of strain KMM 7019T is given in Table 1Go and compared with that of other Salegentibacter species.


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  		Table 1. Cellular fatty acid content (%) of the Salegentibacter species

Fatty acids amounting to less than 1 % of the total in all strains studied are not listed. The fatty acid content of Salegentibacter holothuriorum KMM 3524T was not included in the table because it was determined for bacteria grown under conditions different from those used for the other species. Data are from Nedashkovskaya et al. (2003cGo, 2005)Go and this study. ND, Not detected.

 
A phenotypic analysis was performed using methods described previously (Nedashkovskaya et al., 2003aGo, bGo). API ZYM strips (bioMérieux) and Microlog GN2 plates (Biolog) were also used to assess physiological and biochemical features; these were employed according to the manufacturers' instructions, except that the solution used for the bacterial suspension consisted of 1·5 % NaCl saline, and the strips and the microplates were incubated at 25 °C. Motility was determined as described by Bowman (2000)Go.

The physiological, biochemical and morphological characteristics of strain KMM 7019T are listed in the species description and in Table 2Go. The phenotypic features of the strain tested are consistent with those of the Salegentibacter species (Table 2Go). However, strain KMM 7019T differs from all Salegentibacter species with validly published names by its ability to grow at 41 °C, to hydrolyse agar, to form acid from L-arabinose, D-cellobiose and DL-xylose, to utilize L-arabinose, to move by means of gliding, and by its susceptibility to kanamycin and neomycin. Additional phenotypic traits also distinguish the strain studied from some of the Salegentibacter species (Table 2Go).


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  		Table 2. Phenotypic characteristics of Salegentibacter agarivorans sp. nov. KMM 7019T and other Salegentibacter species

Taxa: 1, Salegentibacter agarivorans sp. nov. (KMM 7019T; this study); 2, Salegentibacter holothuriorum (KMM 3524T; data from Nedashkovskaya et al., 2004Go); 3, Salegentibacter mishustinae (KMM 6049T; data from Nedashkovskaya et al., 2005Go); 4, Salegentibacter salegens (DSM 5424T; data from Dobson et al., 1993Go; McCammon & Bowman, 2000Go; and this study). All strains were positive for the following characteristics: respiratory metabolism; oxidase, catalase, beta-galactosidase and alkaline phosphatase activities; hydrolysis of Tweens 20, 40 and 80, gelatin, elastin, starch and alginic acids; growth at 34 °C and with 8 % NaCl; acid production from D-maltose; utilization of D-glucose and D-mannose; production of H2S; susceptibility to oleandomycin; and resistance to gentamicin and polymyxin B. All strains were negative for the following characteristics: hydrolysis of cellulose (CM-cellulose and filter paper), urea and chitin; acid production from L-rhamnose, L-sorbose, succinate, citrate, glycerol, adonitol, dulcitol, sorbitol, inositoland mannitol; utilization of inositol, mannitol, sorbitol, malonate and citrate; and production of indole and acetoin (Voges–Proskauer reaction).

 
Thus, genomic divergences supported by phenotypic and chemotaxonomic data allow affiliation of strain KMM 7019T to the genus Salegentibacter, in which it forms a distinct lineage, as Salegentibacter agarivorans sp. nov.

Description of Salegentibacter agarivorans sp. nov.
Salegentibacter agarivorans (a.ga.r.i.vo'rans. N.L. n. agarum agar, algal polysaccharide; L. v. vorare to devour, to digest; N.L. part. adj. agarivorans agar-digesting).

Cells are Gram-negative, strictly aerobic, chemo-organotrophic, asporogenic rods 0·5–0·7 µm wide and 2·0–4·7 µm long and motile by gliding. Oxidase-, catalase-, beta-galactosidase- and alkaline phosphatase-positive. Colonies are circular, convex, slimy, shiny with entire edges, sunken into the agar and 1–3 mm in diameter on marine agar 2216. Produces yellow, carotenoid, non-diffusible pigments. Flexirubin-type pigments are absent. Grows in the presence of 1–18 % NaCl; growth optimum observed at 2–4 % NaCl. Growth detected at 4–41 °C, with an optimum at 28–32 °C. The pH range for growth is 5·7–10·0, with optimum growth occurring between pH 7·5 and 8·3. Hydrolyses agar, gelatin, starch, alginic acids, DNA and Tweens 20, 40 and 80, but not casein, cellulose (CM-cellulose and filter paper), chitin or urea. Forms acid from L-arabinose, D-cellobiose, D-fructose, L-fucose, D-galactose, D-glucose, DL-xylose, D-lactose, D-maltose, L-raffinose, D-sucrose and N-acetylglucosamine, but not from L-rhamnose, L-sorbose, adonitol, dulcitol, glycerol, inositol, sorbitol or mannitol. Utilizes D-mannose, but not inositol, sorbitol, mannitol, citrate or malonate. In the Microlog GN2 plate, KMM 7019T utilizes {alpha}-D-glucose, {alpha}-lactose, sucrose, methyl pyruvate, monomethyl succinate, D-galactonic acid, D-gluconic acid, beta-hydroxybutyric acid, p-hydroxyphenylacetic acid, itaconic acid, {alpha}-ketoglutaric acid, DL-lactic acid, propionic acid, succinic acid, succinamic acid, alaninamide, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl L-aspartic acid, L-phenylalanine, L-proline, L-pyroglutamic acid, L-threonine and urocanic acid. Does not utilize {alpha}-cyclodextrin, dextrin, glycogen, N-acetyl-D-galactosamine, adonitol, L-arabitol, i-erythritol, gentiobiose, myo-inositol, lactulose, D-mannitol, D-melibiose, methyl beta-D-glucoside, psicose, D-sorbitol, D-trehalose, turanose, xylitol, acetic acid, cis-aconitic acid, citric acid, formic acid, D-galacturonic acid, D-glucosaminic acid, D-glucuronic acid, {alpha}-hydroxybutyric acid, {gamma}-hydroxybutyric acid, {alpha}-ketobutyric acid, {alpha}-ketovaleric acid, malonic acid, quinic acid, D-saccharic acid, sebacic acid, bromosuccinic acid, glucuronamide, D-alanine, L-alanine, glycyl L-glutamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, D-serine, L-serine, DL-carnitine, {gamma}-aminobutyric acid, inosine, uridine, thymidine, phenylethylamine, putrescine, 2-aminoethanol, 2,3-butanediol, glycerol, DL-{alpha}-glycerol phosphate, glucose 1-phosphate or glucose 6-phosphate. In the API ZYM gallery, KMM 7019T produces {alpha}-galactosidase, beta-galactosidase, alkaline phosphatase, acid phosphatase, esterase lipase (C8), leucine arylamidase, valine arylamidase, trypsin, {alpha}-chymotrypsin, naphthol-AS-BI-phosphohydrolase, {alpha}-glucosidase, beta-glucosidase and N-acetyl-beta-glucosaminidase, but not esterase (C4), lipase (C14), cystine arylamidase, beta-glucuronidase, {alpha}-mannosidase or {alpha}-fucosidase. H2S is produced. Nitrates are reduced to nitrites under oxic conditions. Does not produce indole or acetoin (Voges–Proskauer reaction). Susceptible to chloramphenicol, doxycycline, erythromycin, kanamycin, neomycin, oleandomycin and streptomycin. Resistant to ampicillin, benzylpenicillin, carbenicillin, lincomycin, gentamicin, tetracycline and polymyxin B. The predominant cellular fatty acids are C15 : 1 iso (12·1 %), C15 : 0 iso (12·3 %), C15 : 0 anteiso (7·1 %), C15 : 0 (5·6 %), C17 : 0 iso 3-OH (9·8 %) and summed feature 3 (12·2 %), comprising C16 : 1{omega}7c and/or C15 : 0 iso 2-OH. The DNA G+C content is 39·2 mol%.

The type strain, KMM 7019T (=KCTC 12560T=LMG 23205T), was isolated from a sponge (Artemisina sp.) collected near Onecotan Island, Kuril Islands, Sea of Okhotsk, Pacific Ocean.


   ACKNOWLEDGEMENTS
 
This research was supported by grants from the Federal Agency for Science and Innovations of the Ministry for Education and Sciences of the Russian Federation (nos RI-26/109, 2-2.16 and 112/001/724), the Russian Foundation for Basic Research (no. 05-04-48211) and the Presidium of the Russian Academy of Sciences ‘Molecular and Cell Biology’. K. S. B. acknowledges support from the KRIBB research initiative program. M. V. and J. S. acknowledge the Belgian Federal Public Planning Service – Science Policy.


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