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1 Pacific Institute of Bioorganic Chemistry, Far-Eastern Branch, Russian Academy of Sciences, Prospect 100 Let Vladivostoku 159, 690022 Vladivostok, Russia
2 Tokyo University of Agriculture, Department of Applied Biology and Chemistry, Faculty of Applied Bioscience, Laboratory of Food Science and Technology, Sakuragaoka 1-1-1, Setagaya-ku, Tokyo 156-8502, Japan
3 Department of Medical and Life Science, Faculty of Pharmaceutical Science, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278-8510, Japan
4 Institute of Marine Biology, Far-Eastern Branch, Russian Academy of Sciences, 690041 Vladivostok, Russia
Correspondence
Lyudmila A. Romanenko
lro{at}piboc.dvo.ru
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain KMM 3882T is AB248285.
Tables detailing the antimicrobial properties of strain KMM 3882T and cellular fatty acid profiles of strain KMM 3882T and the type strains of related Sphingomonas species, and figures showing a chromatogram of the polar lipids of strain KMM 3882T and phylogenetic trees based on 16S rRNA gene sequences constructed by using maximum-likelihood and maximum-parsimony are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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and emended subsequently by Takeuchi et al. (2001), Yabuuchi et al. (2002) and Busse et al. (2003). According to Busse et al. (2003), Sphingomonas species comprising cluster I proposed by Takeuchi et al. (2001) should be considered as Sphingomonas sensu stricto, including the type species Sphingomonas paucimobilis.
During the screening of mollusc isolates for antimicrobial activity, strain KMM 3882T was found to have antagonistic effects against a range of Gram-positive indicator bacteria and yeast, but not Gram-negative or fungal cultures. A butanol extract of cellular biomass of strain KMM 3882T was found to have antimicrobial properties against Gram-positive cocci and bacilli (see Supplementary Table S1 in IJSEM Online), pointing to low-molecular-weight metabolites, which could be responsible for the antagonistic activity. Phylogenetic analysis based on 16S rRNA gene sequences demonstrated that strain KMM 3882T belongs to the genus Sphingomonas and may represent a novel species of this genus. Some sphingomonads have been reported to produce the anticyanobacterial compounds argimicins (Yamaguchi et al., 2003) or to be antagonists of phytopathogenic fungi (Berg & Balin, 1994). It should be noted that much more is known about the ability of Sphingomonas strains to degrade organic substances or pollutants, and their biosynthetic production of extracellular polymers (Denner et al., 2001; Balkwill et al., 2003). In the present study, we report the polyphasic characterization of strain KMM 3882T, which was isolated from a marine mollusc, Anadara broughtoni. On the basis of the phenotypic and molecular data obtained, Sphingomonas molluscorum sp. nov. is described.
Strain KMM 3882T was isolated from a marine bivalve specimen (Anadara broughtoni Schrenck 1867), collected from Peter the Great Bay, the Sea of Japan, Russia, in June 2003. The mollusc specimen was carefully rinsed with sterile seawater and cut aseptically with a scalpel. An aliquot of intervalve blood liquor was spread on agar plates of seawater medium (SWM), containing (l–1): 5.0 g peptone, 2.5 g yeast extract, 1.0 g glucose, 0.2 g K2HPO4, 0.05 g MgSO4 and 15.0 g agar in 750 ml seawater/250 ml distilled water. The plates were incubated for 14 days at 28 °C. Strain KMM 3882T grew aerobically on tryptic soy agar (TSA), marine agar 2216 and marine broth (all from Difco) at 28 °C. Strain KMM 3882T was stored at –80 °C in marine broth supplemented with 30 % (v/v) glycerol. Motility was observed by using the hanging drop method. Cell morphology was examined by scanning electron microscopy of exponential phase cells grown in SWM. The Gram-reaction, oxidase and catalase reactions, production of H2S and indole, and hydrolysis of casein, gelatin, starch, chitin, Tween 80, Tween 40 and Tween 20 were tested according to methods described by Smibert & Krieg (1994). The oxidation–fermentation medium of Leifson (1963) was used to test acid production from carbohydrates, with 1 % (w/v) of each compound being used. Growth at various temperatures, pH values and salinities, and substrate utilization were studied as described previously (Romanenko et al., 2003, 2005). In addition, biochemical tests were carried out using API 20NE test kits (bioMérieux), as described by the manufacturer. API test results were read after 24 h and 2 days of incubation at 28 °C.
For fatty acid analysis, strain KMM 3882T was grown on TSA at 28 °C for 48 h. Fatty acid methyl esters (FAMEs) were obtained by using mild alkaline or acid methanolysis, as described by Rowe et al. (2000). The FAMEs were extracted with hexane and analysed by using a GLC-MS Hewlett Packard model 6890 gas chromatograph equipped with an HP 5 MS 5 % Phenyl Methyl Siloxane capillary column (30 mx250 µmx0.25 µm), connected to a Hewlett Packard model 5973 mass spectrometer. Identification of the FAMEs was accomplished by using equivalent chain-length values, comparing the retention times of the samples to those of standards. Lipids were extracted by using the chloroform/methanol extraction method of Bligh & Dyer (1959). The polar lipid composition was determined as described by Denner et al. (2001). Yellow pigments were tested by using TLC (chloroform/methanol, 5 : 3, v/v). The visible spectrum of the acetone extract was examined with a CECIL 7250 spectrophotometer.
To investigate the production of antimicrobial compounds, strain KMM 3882T was cultivated for 48 h at 28 °C on agar slants of SWM supplemented with 0.2 % (w/v) casein hydrolysate. The cells were harvested, suspended in distilled water and subjected to ultrasound for 2 min. The suspension obtained was extracted twice with equal volumes of n-butanol. The organic layers were evaporated to dryness and the residue was diluted in an appropriate amount of ethanol and centrifuged to remove insoluble substances. The cellular extract obtained, referred to as butanol extract, was examined for the presence of antimicrobial activity by using the agar diffusion method. To test for antimicrobial activity, 100 µl butanol extract (100 µg/100 µl, in 10 % ethanol) was placed in wells (9 mm in diameter) cut in nutrient agar plates that had been inoculated with 100 µl of an indicator culture suspension (108 cells ml–1). The plates were incubated at 28 °C for 3 days and examined daily. The formation of a clear inhibition zone around the wells was considered to be indicative of antimicrobial activity. Zones of inhibition were recorded by measuring the clear zone diameter in millimetres, including the 9 mm diameter of the well. All tests were performed in triplicate. The indicator strains used are listed in Supplementary Table S1 in IJSEM Online. Enterococcus faecium CIP 104105 and Staphylococcus aureus CIP 65.8T were obtained from Collection de l'Institut Pasteur (CIP), Paris, France, and the Bacillus species were obtained from the All Russian Collection of Microorganisms (VKM), Pushchino, Russia.
The DNA base composition was determined as described by Marmur & Doty (1962) and Owen et al. (1969). DNA–DNA relatedness was measured by using the photobiotin-labelled DNA probe microplate method of Ezaki et al. (1989). The 16S rRNA gene sequence (1381 bp) of strain KMM 3882T was determined and analysed as described by Shida et al. (1997). The sequence was compared with 16S rRNA gene sequences retrieved from the EMBL/GenBank/DDBJ databases by using the FASTA program (Pearson & Lipman, 1988). Distances were calculated according to the method of Jukes & Cantor (1969). Sequences were aligned using the CLUSTAL W program (Thompson et al., 1994) in the InforBIO software (Sugawara et al., 2003) and putative variable regions, positions 70–100, 181–219, 447–487, 1004–1036, 1133–1141 and 1446–1456 (Escherichia coli numbering system) (Anzai et al., 2000), were eliminated. Phylogenetic trees were constructed by using maximum-likelihood and maximum-parsimony methods with the PHYLIP package (Felsenstein, 1989), and the neighbour-joining method of Saitou & Nei (1987) with the CLUSTAL W program.
Cells of strain KMM 3882T were Gram-negative, aerobic, oxidase- and catalase-positive, yellow-pigmented and non-motile. Physiological, biochemical and chemotaxonomic characteristics of strain KMM 3882T are given in Table 1, in Supplementary Table S2 and Fig. S1 available in IJSEM Online, and in the species description. The predominant polar lipids of strain KMM 3882T comprised phosphatidylcholine (PC), sphingoglycolipid (SGL), phosphatidylglycerol (PG), phosphatidylethanolamine (PE) and diphosphatidylglycerol (DPG). Phosphatidyldimethylethanolamine (PDE), aminolipid and two unknown lipids were also present as minor components (see Supplementary Fig. S1 in IJSEM Online). Two acetone-soluble pigments were found to have the following spectral characteristics: 
max at 426 and 449 nm and a shoulder at 478 nm for the first; and max at 451 and 479 nm and a shoulder at 426 nm for the second. The polar lipid composition of strain KMM 3882T was consistent in its major components, PC, SGL, PG, PE and DPG, with those reported for the closely related species, Sphingomonas trueperi (Kämpfer et al., 1997), Sphingomonas paucimobilis (Kämpfer et al., 1997) and Sphingomonas panni (Busse et al., 2005). Denner et al. (2001) reported for Sphingomonas pituitosa the presence of DPG, PE, PDE, PG, SGL and an unidentified polar lipid as major components and PC, phosphatidylmonomethylethanolamine (PME), aminophospholipid, unknown phospholipids and an unknown glycoplipid as minor components. Strain KMM 3882T could be distinguished from the above-mentioned species and from other recognized Sphingomonas species (Kämpfer et al., 1997; Denner et al., 2001; Busse et al., 2003) by the presence of the minor polar lipid components of unknown lipids and aminolipid and the absence of PME and glycolipids.
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6 (8.1 %), C19 : 1 (3.9 %), C15 : 1 (1.6 %) and the abundance of C18 : 0 (9.2 %). The latter fatty acid was present only in S. azotifigens NBRC 15497T (3.8 %; Xie & Yokota, 2006). Unlike Sphingomonas pituitosa DSM 13101T and Sphingomonas azotifigens NBRC 15497T, strain KMM 3882T did not contain 2-OH C15 : 0. The chemotaxonomic features of strain KMM 3882T, including the presence of sphingoglycolipid, C16 : 0, C18 : 1 and 2-OH C14 : 0 as major fatty acids and the absence of 3-hydroxy fatty acids are in line with the characteristic components reported for recognized species of the genus Sphingomonas (Kämpfer et al., 1997; Takeuchi et al., 2001; Busse et al., 2003).
The DNA G+C content of strain KMM 3882T was 68.3 mol%, which is within the range of values (61.6–68.0 mol%) reported for recognized Sphingomonas species. The value obtained is similar to those determined for recently described Sphingomonas azotifigens strains (66.0–68.0 mol%), but is slightly higher than the values (63.7–65.6 mol%) determined for Sphingomonas pituitosa, Sphingomonas trueperi and the type species Sphingomonas paucimobilis (Table 1
).
On the basis of the morphological and physiological characteristics, polar lipid composition, fatty acid profile and the DNA G+C content, strain KMM 3882T can be considered to be a member of the genus Sphingomonas.
Phylogenetic analysis based on 16S rRNA gene sequences positioned strain KMM 3882T within the genus Sphingomonas as an independent lineage adjacent to Sphingomonas dokdonensis DS-4T (Yoon et al., 2006) and Sphingomonas panni DSM 15761T (Busse et al., 2005) (Fig. 1). The same relationship was also evident in 16S rRNA gene sequence dendrograms based on different treeing algorithms (see Supplementary Figs S1 and S2 in IJSEM Online). Strain KMM 3882T showed the highest 16S rRNA gene sequence similarity of 97.3 % to Sphingomonas dokdonensis DS-4T; similarities of 96.5–96.7 % were obtained with Sphingomonas pituitosa DSM 13101T, Sphingomonas azotifigens NBRC 15497T, Sphingomonas asaccharolytica NBRC 15499T, Sphingomonas trueperi DSM 7225T and Sphingomonas panni DSM 15761T. The 16S rRNA gene sequence similarity value of 97 % is consistent with the criterion for differentiation of bacteria at the species level given by Stackebrandt & Goebel (1994). Relatively low 16S rRNA gene sequence similarity values (96.7 % to Sphingomonas panni DSM 15761T, 96.6 % to Sphingomonas trueperi DSM 7225T and 96.5 % to Sphingomonas pituitosa DSM 13101T, Sphingomonas azotifigens NBRC 15497T and Sphingomonas asaccharolytica NBRC 15499T and values below these to other Sphingomonas species) clearly demonstrated that strain KMM 3882T could be regarded as representing a novel species within the genus Sphingomonas.
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).
The phylogenetic distinction of strain KMM 3882T was supported by its phenotypic characteristics. The phenotypic features of strain KMM 3882T and phylogenetically related species are given in Table 1. Sphingomonas dokdonensis DS-4T was not included because of its recent description (Yoon et al., 2006). Strain KMM 3882T could be distinguished from its close relatives by a combination of phenotypic features. Strain KMM 3882T was similar to Sphingomonas panni in being non-motile, but differed in oxidase reaction and assimilation pattern. Strain KMM 3882T was similar to Sphingomonas trueperi, Sphingomonas paucimobilis (Kämpfer et al., 1997) and Sphingomonas azotifigens (Xie & Yokota, 2006) in being able to assimilate D-glucose, L-arabinose, maltose and N-acetylglucosamine, but differed from all these species in being non-motile and able to assimilate D-gluconate, and from Sphingomonas trueperi and Sphingomonas paucimobilis by not being able to hydrolyse gelatin, and from Sphingomonas paucimobilis and Sphingomonas azotifigens by not being able to hydrolyse starch.
Based on the results obtained, it is proposed that strain KMM 3882T represents a novel species in the genus Sphingomonas, with the name Sphingomonas molluscorum sp. nov.
Description of Sphingomonas molluscorum sp. nov.
Sphingomonas molluscorum (mol.lus.co'rum. N.L. pl. n. Mollusca a zoological phylum; N.L. gen. pl. n. molluscorum of molluscs classified in the phylum Mollusca).
Cells are Gram-negative, non-sporing, non-motile, small rods (0.4–0.6 µm wide and 1.0–1.5 µm long). Form yellow-pigmented, smooth, shining and opaque colonies with regular edges, and 3–4 mm in diameter. Diffusible pigments are not produced. Grows at 7–37 °C, with optimum growth at 25–28 °C. Does not grow at 4 or 42 °C. Sodium ions are not required for growth. Grows in 0–4 % NaCl. Oxidase-, catalase- and 
-galactosidase-positive. Indole, H2S, urease, arginine dihydrolase, ornithine decarboxylase, lysine decarboxylase and phenylalanine deaminase are not produced. Casein, gelatin, starch and chitin are not hydrolysed. Hydrolysis of Tween 80, Tween 40 and Tween 20 is positive. Production of acid from arabinose, galactose and D-xylose is weakly positive. Acid is not produced from D-glucose, rhamnose, maltose, sucrose, lactose, inositol, mannitol or glycerol. Other physiological and biochemical characteristics are given in Table 1. In addition, in API tests, assimilation of mannitol is negative. According to conventional methods, nitrate reduction and utilization of sucrose, inositol, sorbitol and mannitol are negative; utilization of D-glucose, L-arabinose, lactose, D-mannose and malonate is positive. Predominant polar lipids are PC, SGL, PG, PE and DPG. PDE, aminolipid and two unknown lipids are present as minor components. Two acetone-soluble pigments are characterized by max at 426 and 449 nm and a shoulder at 478 nm, and max at 451 and 479 nm and a shoulder at 426 nm. Contains C16 : 0 (24.0 %), C18 : 19 (16.5 %) and C18 : 17c (17.7 %) as major fatty acids and 2-OH C14 : 0 (12.8 %) as a major 2-hydroxy fatty acid; C15 : 0 (1.7 %); C15 : 1 (1.6 %), C16 : 1 (2.1 %), C17 : 1 (2.5 %), C18 : 26 (8.1 %), C18 : 0 (9.2 %) and C19 : 1 (3.9 %) are also present.
The DNA G+C content of the type strain is 68.3 mol% (determined by using the thermal denaturation method). The type strain is KMM 3882T (=An 18T=NRIC 0685T=JCM 14122T=CIP 109223T), which was isolated from a marine bivalve (Anadara broughtoni), collected from Peter the Great Bay, The Sea of Japan, Russia.
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ACKNOWLEDGEMENTS |
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