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1 Department of Biotechnology, Center for Chemistry and Chemical Engineering, Lund University, PO Box 124, SE-221 00 Lund, Sweden
2 Centro de Biotecnología, Facultad de Ciencias y Tecnología, Universidad Mayor de San Simón, Cochabamba, Bolivia
Correspondence
Jorge Quillaguamán
Jorge.Quillaguaman{at}biotek.lu.se
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene of strain LV4T is AY373448.
Transmission electron micrographs of C. sarecensis (strain LV4T), showing that some of the cells become longer and thinner with increasing size, are available as supplementary figures in IJSEM Online.
Present address: PROIMI-CONICET, Avenida Belgrano y Pasaje, Caseros, 4000 Tucumán, Argentina. 
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). The domain Bacteria comprises several representatives that form part of a large number of phylogenetic groups, with distinctive characteristics. The different branches of the Proteobacteria group have various halophilic representatives with close relatives that are non-halophilic (Oren, 2002). Among the bacterial families that form part of the largest subgroup, i.e. the 
-Proteobacteria, the family Halomonadaceae is characterized as being mainly represented by several halophilic and halotolerant species that belong to different genera. Halomonas is the largest genus in this family, containing more than 20 reported species, and is followed by the genus Chromohalobacter, which presently has four species: Chromohalobacter canadensis (Arahal et al., 2001a), Chromohalobacter israelensis (Arahal et al., 2001a), Chromohalobacter marismortui (Ventosa et al., 1989) and Chromohalobacter salexigens (Arahal et al., 2001b). All these species are moderately halophilic, aerobic, motile, Gram-negative, heterotrophic rods. This report describes the phylogenetic and phenotypic characterization of an isolate, LV4T, obtained from a soil sample collected around the saline lake Laguna Verde located in the south-western part of Bolivia (22° 47' 16'' S, 0·67° 49' 55·1'' W) at 4300 m above sea level. Laguna Verde has a typical green coloration (hence its name) owing to the high levels of magnesium in the water. The area around the lagoon is of volcanic origin with environmental temperatures ranging between –15 and 20 °C during the year.
The medium for isolation and maintenance of strain LV4T was modified from that described by Ventosa et al. (1982), being composed of as follows (%, w/v): NaCl, 13·4; MgSO4.7H2O, 0·075; CaCl2.2H2O, 0·03; KCl, 0·15; NaHCO3, 0·005; NaBr, 0·017; proteose-peptone (Difco), 0·5; yeast extract (Difco), 1·0; glucose, 0·1; and granulated agar, 2·0 for solid medium. The pH of the medium was adjusted to 7·5 using 3 M NaOH, to make it similar to that of the soil sample. The isolation procedure consisted of mixing 500 mg soil sample with 0·5 ml medium using gentle vortexing, inoculating 0·2 ml suspension in a 250 ml Erlenmeyer flask containing 100 ml medium, then incubating this at 15 °C with agitation at 200 r.p.m. for 10 days. The enriched bacterial broth was diluted in the sterile liquid medium and then surface-inoculated on solid medium and incubated for 7 days at 18 °C. Finally, the microbial colonies were isolated, taking their morphological differences into consideration.
For taxonomic characterization, strain LV4T was grown in a Casamino acids-based (CAS) medium supplemented with 8 % (w/v) NaCl (Vreeland, 1987) at 30 °C and pH 7·5 (adjusted after sterilization), unless otherwise stated. CAS medium was also previously utilized to characterize three of the species of the genus Chromohalobacter (Huval et al., 1995, Vreeland et al., 1980). Gram staining was performed using a Difco Gram stain set. Colony morphology was analysed according to Smibert & Krieg (1994), after growth for 30 h at 30 °C on CAS solid medium. Bacterial flagella were observed using a JEM-123 (HC) transmission electron microscope by using staining with 2 % uranyl acetate according to Vreeland et al. (1980). Cell size and morphology were examined from 30 h cultures of bacteria using a Nikon optiphot-2 microscope at x1000 magnification. Cell morphology was also observed using a JSM-5600 LV scanning electron microscope (JEOL). For this purpose, cells of strain LV4T were extracted from liquid cultures, washed twice with water and dehydrated through a graded series of ethanol and isopropyl alcohol aqueous solutions. Cells were then mounted on 12 mm cover-slips, dried in a vacuum desiccator overnight and then coated with gold/palladium (80 : 20, w/w).
Acid production by strain LV4T from different carbon sources was analysed as reported by Smibert & Krieg (1994) in a medium containing 1 % (w/v) of a carbon source, 0·3 % (w/v) yeast extract and 9 % (w/v) sea salts (Sigma). Sugar utilization was determined for strain LV4T and C. canadensis using the Biolog GN (for Gram-negative bacteria) MicroPlates system inoculated with 130 µl cell suspension per well. For this purpose, cells were grown in CAS medium for 30 h at 30 °C and suspended in sterile medium containing 5 % (w/v) sea salts (Sigma).
Hydrolysis of starch, Tween 80 and DNA was determined as described previously by Sánchez-Porro et al. (2003). Other biochemical characteristics were screened by using conventional methods according to Smibert & Krieg (1994). In all cases, 9 % (w/v) sea salts (Sigma) was supplied in the medium.
Growth at, and tolerance of, various salt concentrations, temperatures and pH values, respectively, were studied by culturing strain LV4T in 12 ml CAS medium in 50 ml screw-capped bottles (shaken at 200 r.p.m.). For these studies, cells were grown in 0, 5, 8, 10, 15, 25 and 33 % (w/v) NaCl for 10 days, at 0, 4, 15, 25, 30, 35, 45 and 50 °C for 14 days, and at pH 4, 5, 6, 7, 7.5, 8, 9, 10 and 11 (adjusted with 2 M KOH or 2 M HCl) for 10 days. Optical density at 600 nm was monitored, using sterile CAS medium as the reference, with an Ultrospec 3000 spectrophotometer (Pharmacia Biotech). Slopes of optical density against salt concentration, temperature and pH were plotted and the optimal conditions for growth were determined.
Sensitivity to antibiotics was determined using the standard disc assay method (Smibert & Krieg, 1994) in CAS medium supplemented with 8 % (w/v) NaCl, as reported earlier (Huval et al., 1995). The resistance and degree of sensitivity were determined by measuring the sizes of inhibition zones after 30 h incubation at 30 °C in the presence of different amounts of each antibiotic.
Genomic DNA was extracted and purified according to Arahal et al. (2002); its purity was assessed from the A260/A280 and A260/A230 ratios (Johnson, 1994). Universal primers 8-27F (5'-AGAGTTTGATCCTGGCTCAG-3') and 1422 (5'-GGTTACCTTGTTACGACTT-3') were used to amplify the 16S rRNA gene (Weisburg et al., 1991). The PCR products were purified using the QIAquick PCR purification kit (Qiagen) and then resuspended in a final volume of 40 µl. DNA sequencing on both strands was performed by the dideoxy chain-termination method with an ABI prism 3100 DNA analyser, using an ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction kit (PE Biosystems) according to the protocol provided by the manufacturer. GenBank and Ribosomal Database Project databases were used to search for 16S rRNA gene similarities (Maidak et al., 2000). Phylogenetic analysis based on the 16S rRNA gene was performed with the aid of the DNAMAN 4.03 software package, using the neighbour-joining and Jukes–Cantor distance correction methods (Saitou & Nei, 1987). For constructing a phylogenetic tree, only sequences from the type strains of species whose names have been validly published were taken into account. An almost-complete sequence (1450 bp) of the 16S rRNA gene of strain LV4T (GenBank/EMBL/DDBJ accession no. AY373448) was used in the analysis.
Genomic DNA G+C content and DNA–DNA hybridization between strain LV4T and reference strains C. canadensis DSM 6769T and Pseudomonas beijerinckii DSM 7218T, respectively, were determined by the DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen, Braunschweig, Germany). For these assays, DNA was isolated by chromatography on hydroxyapatite by the procedure of Cashion et al. (1977). DNA–DNA hybridization was carried out as described by De Ley et al. (1970), with the modification described by Huss et al. (1983) and Escara & Hutton (1980), using a model 2600 spectrophotometer equipped with a model 2527-R thermoprogrammer and plotter (Gilford Instrument Laboratories). Renaturation rates were computed with the TRANSFER.BAS program of Jahnke (1992). For the determination of G+C content, DNA was hydrolysed with P1 nuclease and the nucleotides dephosphorylated with bovine alkaline phosphatase (Mesbah et al., 1989). The resulting deoxyribonucleosides were analysed by HPLC (Shimadzu equipment) using chromatography conditions adapted from those of Tamaoka & Komagata (1984). The G+C content was calculated from the ratio of deoxyguanosine (dG) and thymidine (dT) according to the method of Mesbah et al. (1989). For these experiments, strain LV4T was grown in CAS medium; reference strains C. canadensis DSM 6769T and P. beijerinckii DSM 7218T were grown according to the conditions given by the DSMZ.
The results of 16S rRNA gene analysis are shown in Fig. 1. Strain LV4T was seen to bear the closest affiliation to C. canadensis DSM 6769T, with sequence similarity of the order of 98·5 %, which is within the mean range reported previously for the genus Chromohalobacter (Arahal et al., 2002).
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; Anzai et al., 2000). Because of the close phylogenetic relationship between P. beijerinckii and the genus Chromohalobacter, its position as another member of this genus should be considered.
Most members of the genus Chromohalobacter were previously considered to belong to the genus Halomonas (Huval et al., 1995; Arahal et al., 2001b), but a re-evaluation of the phylogeny of the species within the family Halomonadaceae, using comparative sequence analysis of the 16S rRNA gene, clustered the Chromohalobacter species in a separate branch from the genus Halomonas (Arahal et al., 2002). In the phylogenetic tree constructed for this report, strain LV4T was grouped together with C. canadensis DSM 6769T and P. beijerinckii DSM 7218T (Fig. 1
), while the Halomonas species having a close phylogenetic affiliation with the genus Chromohalobacter (Arahal et al., 2002) clustered in a separate group.
Table 1 provides a comparison of the taxonomic features of strain LV4T with those of other Chromohalobacter species. Cells of strain LV4T are aerobic and motile by means of a polar flagellum. Moreover, strain LV4T is a Gram-negative, rod-shaped organism and the cells occur singly or occasionally in pairs. Strain LV4T cells exhibit a wide range of sizes during the exponential phase of growth, ranging from short rods with a coccoid form to sporadically elongated cells that become thinner with increasing size (see supplementary figures in IJSEM Online). With respect to its nutritional and biochemical characteristics, strain LV4T showed some similarity to the reference Chromohalobacter species, but differences were also noted. Like the other Chromohalobacter species, strain LV4T is a heterotrophic bacterium able to assimilate a diverse range of carbon sources; however, the substrates it can assimilate differ from those assimilated by C. canadensis (Table 1). The ability of some Chromohalobacter species to reduce nitrate was not found in strain LV4T (Table 1). Furthermore, resistance to lysis in water, the absence of indole production and the presence of oxidase activity are other features that differentiate strain LV4T from C. canadensis DSM 6769T (Table 1).
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). In contrast to C. canadensis DSM 6769T, strain LV4T does not require added NaCl to grow in CAS medium (Huval et al., 1995) (Table 1). Although the composition of the medium may influence the salt tolerance and requirement in halophilic bacteria (Ventosa et al., 1998), growth without NaCl is a characteristic of strain LV4T not shared with C. canadensis under the same culture conditions. Strain LV4T grows at temperatures from 0 °C (the lowest temperature tested) up to 45 °C and exhibits optimal growth between 30 and 35 °C: thus it can be classified as psychrotolerant according to the definition by Morita (1975). A minimum growth temperature of 4 °C was determined previously for C. marismortui and C. salexigens (Table 1); only slight growth was reported for the latter organism at that temperature (Vreeland et al., 1980). Cell growth was observed over a broad range of pH values (5–10), with optimum growth occurring at pH 7·5–8·0. The growth of strain LV4T cells was inhibited by ampicillin, chloramphenicol and tetracycline, in all cases at a minimum level of 10 µg. However, the organism did not show susceptibility to penicillin G (50 IU), streptomycin (50 µg) or kanamycin (80 µg).
Analysis of strain LV4T genomic DNA revealed its G+C content to be 56·1 mol%, differing significantly from that of the other Chromohalobacter species (Table 1). Nevertheless, it should be pointed out that different values for the G+C content of C. canadensis have been reported in different studies (Huval et al., 1995; Arahal et al., 2001a). The DNA–DNA relatedness values obtained for strain LV4T with respect to C. canadensis DSM 6769T and P. beijerinckii DSM 7218T were 47·9 and 32·8 %, respectively. These DNA similarities are lower than the recommended value of at least 70 % accepted as the definition of a novel species (Wayne et al., 1987).
Because of the taxonomic differences listed, the marked difference in the G+C content, the low DNA–DNA hybridization values for strain LV4T with respect to the species showing the closest 16S rRNA gene similarity, and the novel characteristics shown by strain LV4T, we propose that this strain represents a novel member of the genus Chromohalobacter, with the name Chromohalobacter sarecensis sp. nov.
Description of Chromohalobacter sarecensis sp. nov.
Chromohalobacter sarecensis (sa.re.cen'sis. N.L. masc. adj. relating to Sida/SAREC, the institution that supports scientific research in Bolivia).
Aerobic, Gram-negative and motile by means of a polar flagellum. The DNA G+C content is 56·1 mol%. Cells are rod-shaped and 0·5x0·8 to 0·8x6·1 µm in size. Cells occur singly or in pairs and show a wide distribution of sizes during the exponential phase of growth. Colonies are circular with entire margins, convex, smooth with a glistening surface and have a translucent to brown pigment, which is enhanced in old cultures. Acid is produced in medium supplied with fructose, xylose, glucose, rhamnose, galactose or glycerol, but acidification is not detected with trehalose, sucrose, citrate or raffinose. Heterotrophic and able to oxidize L-arabinose, D-arabitol, iso-erythritol, D-galactose, D-mannitol, D-mannose, D-psicose, raffinose, rhamnose, D-sorbitol, xylitol, lactose, cellobiose, glucose, ribose, D-xylose, melibiose, acetic acid, cis-aconitic acid, citric acid, formic acid, D-galactonic acid, D-gluconic acid, DL-lactic acid, succinic acid, bromosuccinic acid, L-alanine, D-alanine, L-alaninamide, L-alanylglycine, L-asparagine, L-aspartic acid, L-proline, L-pyroglutamic acid, L-serine and glycerol. Cells are unable to metabolize 
-cyclodextrin, dextrin, glycogen, adonitol, L-fucose, gentibiose, myo-inositol, turanose, pyruvic acid methyl ester, D-galacturonic acid, D-glucosaminic acid, D-glucuronic acid, itaconic acid, -ketoglutaric acid, malonic acid, quinic acid, D-saccharic acid, sebacic acid, succinamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, L-phenylalanine, D-serine, L-threonine, urocanic acid, inosine, uridine, thymidine, putrescine, 2-aminoethanol or 2,3-butanediol. Catalase-, oxidase- and tryptophan deaminase-positive. Indole and sulfide are not produced, nitrate is not reduced, caseinase, DNase and urease are not present and gelatin is not liquefied. Tests for hydrolysis of Tween 40, Tween 80, starch and aesculin are negative. Moderately halophilic and psychrotolerant bacterium: grows at 0–25 % (w/v) NaCl in CAS medium, with the optimum at 8 % (w/v) NaCl; grows at 0–45 °C, with the optimum between 30 and 35 °C; grows at pH 5–10, with the optimum between pH 7·5 and 8·0.
The type strain is LV4T (=CCUG 47987T=ATCC BAA-761T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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