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Microbial Exopolysaccharide Research Group, Department of Microbiology, Faculty of Pharmacy, Campus Universitario de Cartuja, University of Granada, 18071 Granada, Spain
Correspondence
Victoria Béjar
vbejar{at}ugr.es
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7c (68·9 %) and 19 : 0 cyclo 8c (12·8 %). The sole respiratory lipoquinone found in strain B33T is ubiquinone-10. The DNA G+C content is 64·2 mol%. 16S rRNA gene sequence comparisons show that the isolate is a member of the Roseobacter clade within the class ‘Alphaproteobacteria’. The similarity values with Roseivivax halodurans and Roseivivax halotolerans are 88·2 and 88·0 % respectively and 92·2 % with Salipiger mucosus. DNA–DNA hybridization values with these species are <30 %. In the light of the polyphasic evidence gathered in this study it is proposed that the isolate be classified as a novel genus and species with the name Palleronia marisminoris gen. nov., sp. nov. The proposed type strain is strain B33T (=CECT 7066T=LMG 22959T).
-hydroxyalkanoatePublished online ahead of print on 16 September 2005 as DOI 10.1099/ijs.0.63906-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Palleronia marisminoris B33T is AY926462.
A more detailed phylogenetic tree based on 16S rRNA gene sequences is available as a supplementary figure in IJSEM Online.
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). They are widely distributed among many hypersaline habitats. Taxonomically the majority of Gram-negative halophilic bacteria belong to the class ‘Gammaproteobacteria’ but they can also be found in other bacterial phyla (Ventosa et al., 1998). Some halophilic micro-organisms, such as those which produce exopolysaccharides (EPS), have interesting industrial applications (Quesada et al., 2004). Microbial EPS have a potentially wide range of applications in such fields as pharmacy, foodstuffs, cosmetics and the petroleum industry, where emulsifying, viscosifying, suspending and chelating agents are required (Sutherland, 1990). During an extensive search of 18 hypersaline habitats in Spain and Morocco, designed to obtain new EPS, we discovered that the commonest halophilic EPS-producers were various species of the genus Halomonas, most importantly Halomonas maura and Halomonas eurihalina (Quesada et al., 1990, 2004; Bouchotroch et al., 2001; Martínez-Cánovas et al., 2004d). As a result of these searches we have described the first moderately halophilic EPS-producing micro-organism belonging to the ‘Alphaproteobacteria’, Salipiger mucosus (Martínez-Cánovas et al., 2004e), three novel Halomonas species, Halomonas ventosae (Martínez-Cánovas et al., 2004c), Halomonas anticariensis (Martínez-Cánovas et al., 2004a) and Halomonas almeriensis (Martínez-Checa et al., 2005a), two new Idiomarina species, Idiomarina fontislapidosi and Idiomarina ramblicola (Martínez-Cánovas et al., 2004b), and a new Alteromonas species, Alteromonas hispanica (Martínez-Checa et al., 2005b), all of which produce EPS. We describe and classify here an unassigned halophilic EPS-producing strain also isolated in these studies and propose it as a novel genus and species belonging to the class ‘Alphaproteobacteria’ with the name Palleronia marisminoris.
The strain in question, B33T, was isolated from a saline soil bordering a saltern on the Mediterranean seaboard at Marchamalo (Murcia, south-eastern Spain) (Martínez-Cánovas et al., 2004d). It was routinely grown at 32 °C in MY medium (Moraine & Rogovin, 1966) supplemented with a 5 % w/v sea-salt solution (Rodríguez-Valera et al., 1981). Its phenotype was studied with 135 tests by Martínez-Cánovas et al. (2004d) and it was included in phenon E along with other unidentified strains. The procedures we followed for its phenotypic characterization have been described by Ventosa et al. (1982), Quesada et al. (1983) and Mata et al. (2002). Salt requirements and optimum salt concentration were determined in MY medium (Moraine & Rogovin, 1966). The salt concentrations assayed ranged from 0·5 to 30 % w/v and were prepared from a mixture of sea salts according to Rodríguez-Valera et al. (1981). We also tested to see whether strain B33T could survive with NaCl alone or whether it required other sea salts. To determine its nutritional requirements we also assayed its growth in Koser medium supplemented with yeast extract (0·1–3 % w/v), malt extract (1–3 % w/v) or proteose peptone (1–5 % w/v). The presence of bacteriochlorophyll a was analysed spectrophotometrically using the procedure of Cohen-Bazire et al. (1957), following the recommendations of Allgaier et al. (2003). DNA was purified using the technique of Marmur (1961). The G+C content of the DNA was estimated from the midpoint value (Tm) of the thermal denaturation profile (Marmur & Doty, 1962). Tm was determined by the graphic method described by Ferragut & Leclerc (1976) and the DNA G+C content was calculated from this temperature using Owen and Hill's equation (Owen & Hill, 1979). The Tm value of reference DNA from Escherichia coli NCTC 9001T was taken to be 74·6 °C in 0·1x SSC (Owen & Pitcher, 1985).
The phenotypic characteristics and DNA G+C content are given in the species description. Phenotypic features that distinguish between strain B33T, S. mucosus and the two species of Roseivivax are available in Table 1, where it can be seen that strain B33T is phenotypically most closely related to S. mucosus. Both species are Gram-negative, non-motile, moderately halophilic rods. They are chemoheterotrophic, strictly aerobic and produce EPS. They do not produce bacteriochlorophyll a. They do not produce acids from sugars and have low nutritional versatility as they cannot grow with any of the carbohydrates, alcohols, organic acids or amino acids tested as sole sources of carbon and energy. For optimum growth strain B33T requires yeast extract (0·3 % w/v), malt extract (0·3 % w/v) and proteose peptone (0·5 % w/v) together with Na+ (0·66 M), Mg2+ (0·1 M) and K+ (0·01 M), and thus it flourishes in an MY complex medium (Moraine & Rogovin, 1966) supplemented with 5 % w/v sea salts. The most important phenotypic tests distinguishing between Palleronia marisminoris B33T and S. mucosus are pigment production, a negative reaction for oxidase, urease and gluconate oxidation, positive reaction for ONPG and an inability to grow with NaCl alone. The DNA G+C content of strain B-33T (64·2 mol%) is very similar to those of S. mucosus and R. halodurans (64·5 and 64·4 mol%, respectively).
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). Strain B33T contains a large quantity of cis-11 octadecenoic acid (18 : 17c) (68·9 %) together with 19 : 0 cyclo 8c, 3-hydroxy 10 : 0, 16 : 0 and 18 : 0 (12·8, 5, 4·2 and 3·4 % respectively). It also has 2·3 % of an unknown component at a retention time of 4·870 min. The presence of 18 : 17c as the predominant fatty acid is a feature characteristic of taxa within the ‘Alphaproteobacteria’. Nevertheless, the cyclo-substituted fatty acid (19 : 0 cyclo 8c) is not widely present in the family ‘Rhodobacteraceae’; though it has been described in lesser quantities (2·2 %) in S. mucosus. The only respiratory lipoquinone detected was ubiquinone-10. The presence of ubiquinone-10 as the dominant respiratory lipoquinone is characteristic of members of the ‘Alphaproteobacteria’.
The transmission electron micrograph (Fig. 1), prepared using the methods described by Bouchotroch et al. (2001), shows the cell morphology of strain B33T. Thin sections reveal a typical Gram-negative cell-envelope profile; the cell contains poly--hydroxyalkanoate (PHA) granules. EPS appears in the external medium.
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). The forward primer was 16F27 (5'-AGAGTTTGATCMTGGCTCAG-3'), annealing at positions 8–27, and the reverse primer was 16R1488 (5'-CGGTTACCTTGTTAGGACTTCACC-3'), annealing at the complement of positions 1511–1488 (E. coli numbering according to Brosius et al., 1978). The PCR products were purified using the Qiaquick spin-gel extraction kit (Qiagen). Direct sequence determinations of PCR-amplified DNAs were carried out with the ABI PRISM dye-terminator, cycle-sequencing, ready-reaction kit (Perkin-Elmer) and an ABI PRISM 377 sequencer (Perkin-Elmer) according to the manufacturer's instructions. The sequences obtained were compared with reference 16S rRNA gene sequences available in the GenBank/EMBL/DDBJ databases obtained from the National Center of Biotechnology Information database using the BLAST search. Phylogenetic analysis was made using the software MEGA version 3.0 (Kumar et al., 2004) after multiple alignments of data by CLUSTAL_X (Thompson et al., 1997). Distances and clustering were determined with the neighbour-joining and maximum-parsimony methods. The stability of the clusters was ascertained by performing a bootstrap analysis (1000 replications). Our phylogenetic analysis with the neighbour-joining method included, along with the sequence of B33T, some representatives of the family ‘Rhodobacteraceae’ (Fig. 2 and Supplementary Fig. S1 in IJSEM Online). The maximum-parsimony algorithm gave a similar result (data not shown). Strain B33T showed 92·2 % 16S rRNA gene sequence similarity with S. mucosus. Other phylogenetically close species were Roseivivax halodurans and Roseivivax halotolerans, with which it showed 88·2 and 88·0 % sequence similarity, respectively. Strain B33T is in the same clade as Roseivivax and Salipiger, belonging to the 
-3 group of the ‘Alphaproteobacteria’ within the family ‘Rhodobacteraceae’ (Garrity et al., 2001). Roseivivax is taxonomically related to the Roseobacter clade, a group of genera of the family ‘Rhodobacteraceae’ (Allgaier et al., 2003), which make up the most abundant population in marine habitats (González & Moran, 1997).
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) with the modifications of Ziemke et al. (1998) and Bouchotroch et al. (2001). DNA–DNA hybridization values of B33T with the most phylogenetically related species, R. halodurans, R. halotolerans and S. mucosus, are 22, 27·7 and 29·7 %, respectively. Thus, on the basis of phylogenetic evidence, DNA–DNA hybridization values, fatty-acid profiles, quinones, differences in phenotypic characteristics and its inability to synthesize bacteriochlorophyll a, we are of the opinion that strain B33T should be recognized as the representative species of a novel genus, for which we propose the names Palleronia and Palleronia marisminoris.
Description of Palleronia gen. nov.
Palleronia (Pall.er.o'nia. N.L. sb. f. Palleronia in honour of Professor Norberto Palleroni, a pioneer in the use of molecular identification techniques in prokaryote taxonomy).
Gram-negative, short, non-motile rods, 2–2·5 µm long by 0·75–1 µm wide. Neither flagella nor endospores are present. Bacteriochlorophyll a is absent. Metabolism is chemoheterotrophic and aerobic, the cells being unable to grow under anaerobic conditions either by fermentation, nitrate or fumarate reduction or photoheterotrophy. PHA and catalase are present. Oxidase test is negative. Colonies contain pink pigment. The bacteria cannot produce acids from sugars and have low nutritional and biochemical versatility. They are strictly halophilic, requiring Na+, Mg2+ and K+ for growth. The principal cellular fatty acids are 18 : 17c and 19 : 0 cyclo 8c. They have ubiquinone with ten isoprene units. The type species is Palleronia marisminoris.
Description of Palleronia marisminoris sp. nov.
Palleronia marisminoris (ma'ris.min.or.is. L. sb. n. gen. maris of the sea; L. adj. n. gen. minoris smaller; L. adj. marisminoris of the smaller sea, i.e. from el Mar Menor, a shallow area of sea highly sheltered from the Mediterranean sea on the south-eastern coast of Spain, from whence the type strain was isolated).
In addition to the traits reported for the genus, the species grows on MY solid medium in the form of circular, convex, pink, mucoid colonies. In liquid medium its growth pattern is uniform. The cells are encapsulated. It is moderately halophilic, capable of growing in salt concentrations (mixture of sea salts) from 0·5 to 15 % w/v. Optimum growth occurs at 5 % w/v sea salt. It cannot grow with NaCl as the sole salt. Minimum salt requirements are 0·66 M Na+, 0·1 M Mg2+ and 0·01 M K+. It grows within the temperature range of 20 to 37 °C and at pH values of between 5 and 10. It produces H2S from L-cysteine. Selenite reduction and phosphatase tests are positive. Tween 20 is hydrolysed. It does not produce acids from the following sugars and related compounds: adonitol, D-cellobiose, D-fructose, D-galactose, D-glucose, myo-inositol, lactose, maltose, D-mannitol, D-mannose, D-melezitose, L-rhamnose, sucrose, D-salicin, D-sorbitol, sorbose and D-trehalose. ONPG is positive. O/F, indole, methyl-red, Voges–Proskauer and gluconate oxidation are negative. Phenylalanine deaminase is not produced. Urea, tyrosine, Tween 80, starch, aesculin, gelatin, DNA, lecithin and casein are not hydrolysed. Growth on either MacConkey or cetrimide agar is inviable. Blood is not lysed. Neither nitrate nor nitrite is reduced. The following compounds are not acceptable as sole carbon and energy sources: L-arabinose, D-cellobiose, aesculin, D-fructose, glucose, galactose, lactose, maltose, D-mannose, D-salicin, trehalose, acetate, citrate, formate, fumarate, gluconate, lactate, malonate, propionate, succinate, adonitol, ethanol, glycerol, inositol, mannitol and sorbose. The following compounds are not used as sole carbon, nitrogen and energy sources: L-alanine, L-cysteine, D-histidine, isoleucine, L-lysine, L-methionine, L-serine, tryptophan and L-valine. It is susceptible to (µg) amoxicillin (25), ampicillin (10), carbenicillin (100), cefotaxime (30), cefoxitin (30), chloramphenicol (30), erythromycin (15), kanamycin (30), streptomycin (10), nitrofurantoin (300), rifampicin (30) and tobramycin (10) and is resistant to nalidixic acid (30), polymyxin B (300) sulfonamide (250) and trimethoprim/sulfamethoxazole (1·25/23·7). The major fatty acids are: 18 : 17c (68·9 %), 19 : 0 cyclo 8c (12·8 %), 3-hydroxy 10 : 0 (5 %), 16 : 0 (4·2 %), 18 : 0 (3·4 %). DNA G+C content is 64·2 mol% (Tm method).
The type strain, strain B33T (=CECT 7066T=LMG 22959T), was isolated from a hypersaline soil bordering a solar saltern in Marchamalo (Murcia, south-eastern Spain).
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ACKNOWLEDGEMENTS |
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