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Istituto di Chimica Biomolecolare, Comprensorio ex Olivetti, via Campi Flegrei 34, 80078 Pozzuoli, Napoli, Italy
Correspondence
Assunta Giordano
agiordano{at}icmib.na.cnr.it
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, 2005a, b). Recent studies have clearly shown that halophilic and alkaliphilic species are good sources of biomolecules of industrial interest (Ito et al., 1998; Margesin & Schinner, 2001; Berkeley et al., 2002), particularly for the production of exopolysaccharides and biosurfactants (Horikoshi, 1999; Oren, 2002a, b) or compatible solutes (Sauer & Galinski, 1998), and enzymes of biotechnological interest, such as proteases for use in the paper-pulp industry and for inclusion in laundry detergents (Demirjian et al., 2001; Sanchèz-Porro et al., 2003). The isolates from Campania springs possessed enzymes of interest such as glycosidases and proteases and produced endo- and exopolymers of industrial interest (Romano et al., 2003, 2005a, b).
The genus Oceanobacillus was created by Lu et al. (2001) to allocate some alkaliphilic isolates and a second species was recently accommodated in the genus (Yumoto et al., 2005). In this study, a new member of the genus Oceanobacillus is proposed on the basis of polyphasic studies.
Strain 20AGT was isolated by the dilution-plating technique from an algal mat (pH 8·0, 27 °C) collected from a sulfurous spring in the Santa Maria Incaldana site (Mondragone, Caserta Province, Campania Region, southern Italy). Strain 20AGT was the predominant organism in the enrichment and was the only colony-forming organism at the highest dilutions. The enrichment medium (medium 1) contained the following components (l–1): Na2CO3, 3·0 g; KCl, 2·0 g; MgSO4.7H2O, 1·0 g; NaCl, 100 g, trisodium citrate, 3·0 g; yeast extract, 10·0 g; MnCl2.4H2O, 0·36 mg; FeSO4, 50 mg. Na2CO3 and NaCl were autoclaved separately. The pH of medium 1 was 9·0. Growth on single carbon sources was tested in a liquid medium (medium 2) containing the following (l–1): K2HPO4, 7·0 g; KH2PO4, 2·0 g; MgSO4.7H2O, 0·1 g; (NH4)2SO4, 1·0 g; NaCl, 100 g; Na2CO3, 3·0 g; thiamine hydrochloride solution (500 µl; final concentration 100 mg l–1); each tested compound was added at 10·0 g l–1. Solid media were prepared by the addition of 1·8 % agar. Growth under anaerobic conditions was examined as previously reported (Jeanthon et al., 1995).
Cell morphology was determined by phase-contrast microscopy (Zeiss). Colony morphology was analysed on solid medium by using a Leica M8 stereomicroscope. Tolerance of NaCl and growth at various temperatures and pH values were determined in medium 1. All growth tests were done at the optimal growth temperature (37 °C) for 3 days. Sensitivity of the strain to antibiotics was tested by using medium 1 with agar (1·8 %) and Sensi discs (6 mm; Oxoid); tests were incubated for 48 h. The antibiotic tests were carried out according to Romano et al. (1993). Casein (5 %) and gelatin (12 %) hydrolysis and oxidase, tyrosinase, aminopeptidase (Bactident; Merck) and catalase activities were tested in medium 1. For nitrate reduction, medium 1 plus 0·1 % KNO3 was employed. Hydrolysis of hippurate was examined in medium 1 plus hippurate (1 %) (Romano et al., 1996). For the indole test, strain 20AGT was grown at pH 8·0 in a medium containing all the above-mentioned components without Na2CO3. Gram-staining was performed according to Dussault (1955). The KOH test was performed according to Halebian et al. (1981). Hydrolysis of N'-benzoylarginine p-nitroaniline (BAPNA) stereoisomers was tested according to Oren & Galinski (1994). Extraction of intracellular solutes and their purification and quantification were performed according to Motta et al. (2004). Cells for exopolysaccharide studies were grown on minimal medium. For exopolysaccharide recovery, cells were harvested in the stationary growth phase and the supernatants were treated and analysed as reported by Manca et al. (1996) and Nicolaus et al. (2004).
Cell mass for quinone and lipid analysis was obtained from culture in medium 1 at 37 °C, pH 9·0, at the optimal NaCl concentration (10 %). Lipid analysis was performed as reported by Romano et al. (2001). Lipid hydrolysis and identification of fatty acid methyl esters were performed as reported by Romano et al. (2001). Quinones were analysed by LC/MS on a reversed-phase column by EI/MS and H1 NMR spectrum analysis. The G+C content was determined by the method of Tamaoka & Komagata (1984); DNA was hydrolysed and the resultant nucleotides were analysed by HPLC. The DNA was isolated as previously described (Romano et al., 2003).
The total 16S rRNA gene sequence was determined by direct sequencing of the PCR product. Genomic DNA extraction, amplification of the 16S rRNA gene and purification of the PCR products were carried out as described previously (Romano et al., 2003). Purified PCR products were sequenced by the DSMZ using the ABI PRISM Dye Terminator cycle sequencing ready reaction kit (Applied Biosystems) as directed by the manufacturer. Sequence reactions were electrophoresed using an Applied Biosystems 373A DNA sequencer.
The multiple sequence alignment program CLUSTAL W (Chenna et al., 2003) was used to align the 16S rRNA gene sequence obtained in this study and sequences of organisms belonging to the genus Bacillus and related genera showing the highest sequence similarity. Sequences of 16S rRNA genes for comparison were obtained from the EMBL database (http://www.ebi.ac.uk/fasta33/index.html) or RDP (http://www.ebi.ac.uk/Tools/similarity.html). Phylogenetic analysis based on the 16S rRNA gene sequence by the neighbour-joining method (distance options according to Kimura two-parameter model) was performed using the PHYLIP package, version 3.6 (Felsenstein, 2004). Clustering with the maximum-parsimony method was made by using bootstrap values based on 100 replications. DNA–DNA hybridization was performed by the DSMZ between strain 20AGT and O. iheyensis DSM 14371T and O. oncorhynchi NCIMB 14022T (kindly supplied by I. Yumoto and grown according Yumoto et al., 2005). The DNA was isolated as described previously (Romano et al., 2003).
16S rRNA gene phylogenetic analysis, based on the neighbour-joining method (Saitou & Nei, 1987), showed the position of strain 20AGT in the genus Oceanobacillus (Fig. 1). In particular, the sequence similarity to any other species with validly published names within the genera Bacillus, Virgibacillus, Halobacillus and Gracibacillus was less than 96 %. The G+C content of the DNA was determined to be 40·1 mol%.
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-linked disaccharides such as trehalose and maltose. Among the antibiotics tested, strain 20AGT was sensitive to (µg) erythromycin (5), penicillin G (2), chloramphenicol (10), bacitracin (10), tetracycline (50), lincomycin (15), vancomycin (30), ampicillin (25), novobiocin (30) and streptomycin (25) and resistant to kanamycin (30) and tetracycline (30).
The total lipid content of strain 20AGT accounted for 9–11 % of the total dry weight of cells grown under optimal growth conditions in medium 1 and, under these conditions, phosphatidylglycerol and phosphatidylcholine were the main lipids (approx. 95 %), identified by 1H and 13C NMR. The chemical shifts of signals present in spectra were similar to those reported by Romano et al. (2003), with the exception of the absence of signals due to double bonds in the fatty acid chains. Assignments were made by comparison with commercial standards and by DEPT (distortionless enhancement by polarization transfer) experiments. Glycolipids were not visualized.
The fatty acid composition determined for cells grown under standard growth conditions was characterized by the abundance of branched saturated acyl chains; in particular, ai-C14, i-C15 : 0 and ai-C15 : 0 made up about 90 % of total fatty acid methyl esters. i-C14 : 0, C15 : 0, C16 : 1, C17 : 0 and ai-C18 : 0 each made up less than 0·5 %, while C16 : 0, i- and ai-C17 : 0 and i-C18 : 0 constituted about 9·0 % of the total fatty acids. The high level of branched fatty acids present in strain 20AGT was similar to results for the other two species of the genus Oceanobacillus and members of Virgibacillus, Halobacillus and Bacillus (Heyrman et al., 1999, 2003; Lu et al., 2001).
LC/MS as well as EI/MS analyses of the quinone content of strain 20AGT showed a major peak assigned to MK-7, as was found in O. iheyensis DSM 14371T (Lu et al., 2001).
Little effort has been devoted to the study of osmoprotectants accumulated by halophilic Gram-positive bacteria; under optimal growth conditions, strain 20AGT accumulated glycine betaine and glutamate. In minimal medium containing trehalose (10 g l–1), strain 20AGT produced 9 mg exopolysaccharide l–1.
The two species of the genus Oceanobacillus are halotolerant and alkaliphilic. Strain 20AGT could be considered as moderately halophilic and alkalitolerant, requiring at least 5 % NaCl in the medium for growth and 10 % NaCl for optimal growth, while the existing species of the genus can grow in the absence of NaCl and the optimal NaCl concentration was 3·0 and 7·0 % for O. iheyensis DSM 14371T and O. oncorhynchi NCIMB 14022T, respectively. O. oncorhynchi NCIMB 14022T is an obligate alkaliphile in that it is not able to grow at pH below 9·0, while isolate 20AGT can grow at a slightly acidic pH (6·5). Among the differential phenotypic characteristics of strain 20AGT and the closely related O. oncorhynchi NCIMB 14022T was their different behaviour when the strains were grown under anaerobic conditions; O. oncorhynchi NCIMB 14022T was able to grow under anaerobiosis, while 20AGT was not. Other differential properties were morphology, in that cells of strain 20AGT are longer than those of O. oncorhynchi NCIMB 14022T, the absence of spore formation in 20AGT, the ability of 20AGT to hydrolyse p-nitrophenyl -D-glucopyranoside (PNPG) and the fatty acid composition (20AGT possesses C14 instead of C17 as one of the main components of the fatty acid mixture). Characteristics that differentiate strain 20AGT and O. oncorhynchi NCIMB 14022T are summarized in Table 1.
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. However, their nearly identical 16S rRNA gene sequences (99·5 % similarity), DNA–DNA relatedness above 50 % and the paucity of phenotypic differences did not allow us to assign strain 20AGT to a novel species of the genus Oceanobacillus; instead, we propose to assign it as a subspecies of O. oncorhynchi, on the basis of recent recommendations about the species concept for prokaryotes (Rosselló-Mora & Amman, 2001; Stackebrandt et al., 2002).
The genus Oceanobacillus was created by Lu et al. (2001, 2002) and at the time of writing contains only two species, O. iheyensis (whose entire genome sequence has been determined and is now available; Takami et al., 2002) and O. oncorhynchi, the description of which was published online while this paper was under review (Yumoto et al., 2005). Recently, Caton et al. (2004) found several Oceanobacillus strains in the Salt Plains National Wildlife Refuge in Oklahoma, USA. In particular, one of them, strain GSP73 (GenBank accession number AY553089), showed 99·9 % 16S rRNA gene sequence similarity to strain 20AGT. Some general phenotypic features were reported on the Salt Plains Microbial Observatory database (http://www.okstate.edu/artsci/SPMO/). This isolate, like the two described species of Oceanobacillus, is not halophilic but halotolerant in that it was able to grow in the absence of NaCl and required 8·0 % NaCl for optimal growth. Finally, in the EMBL database, the sequence AB189328 of an unidentified and undescribed isolate Oceanobacillus sp. JM-Ob showed 100 % 16S rRNA gene sequence similarity with strain 20AGT. Strains GSP73, JM-Ob and 20AGT could be classified as members of the same subspecies after further studies. Strain 20AGT should be designated as the type strain of a novel subspecies, for which the name Oceanobacillus oncorhynchi subsp. incaldanensis subsp. nov. is proposed. According to Rule 40b of the Bacteriological Code, the creation of this subspecies automatically creates the subspecies Oceanobacillus oncorhynchi subsp. oncorhynchi subsp. nov.
Emended description of Oceanobacillus oncorhynchi Yumoto et al. 2005
Oceanobacillus oncorhynchi (on.co.rhyn'chi. N.L. gen. n. oncorhynchi of Oncorhynchus, named after the rainbow trout, Oncorhynchus mykiss, from which the type strain was isolated).
Cells are Gram-positive, peritrichously flagellated, straight rods, 0·4–0·8x1·1–2·0 µm. Colonies are circular and white or beige. Ability to produce ellipsoidal spores is variable. Obligate or facultative alkaliphile; obligate or facultative halophile. Ability to grow under anaerobic conditions is variable. Growth occurs at 10–40 °C with optimum growth at 30–37 °C. Growth occurs at 0–22 % NaCl with optimum growth at 7–10 %. Nitrate may be reduced to nitrite. The DNA G+C content is 38·5–40·1 mol%. Able to produce 
-glycosidase and exopolysaccharide. Branched fatty acids from C14 : 0 up to C18 : 0 are the major components; traces of unsaturated fatty acids are also found. The type strain is strain R-2T (=JCM 12661T=NCIMB 14022T).
Description of Oceanobacillus oncorhynchi subsp. incaldanensis subsp. nov.
Oceanobacillus oncorhynchi subsp. incaldanensis (in.cal.da.nen'sis. N.L. masc. adj. incaldanensis pertaining to the Incaldana site, southern Italy, where the type strain was isolated).
Alkalitolerant, moderately halophilic and obligately aerobic. Cells are regular, motile, non-sporulating rods, 0·5–0·8x1·2–2·0 µm. Colonies are beige. Mesophilic, exhibiting optimum growth at 37 °C, but able to grow at 10–40 °C and at pH 6·5–9·5 (optimum pH 9·0). Grows at salinity of 5–20 % (w/v), with optimum growth at 10 % (w/v) NaCl. Able to grow on D-glucose, D-galactose, D-fructose, D-mannose, D-arabinose, D-sorbose, D-ribose, D-xylose, sucrose, maltose, cellobiose, D-lactose, trehalose, glycerol, sodium acetate and trisodium citrate as sole carbon sources. Positive for the KOH test, oxidase, catalase and reduction of nitrate to nitrite, and negative with respect to aminopeptidase test, hydrolysis of starch, casein and gelatin, urease and indole production. The main menaquinone type is MK-7 and the predominant polar lipids are phosphatidylglycerol and phosphatidylcholine. ai-C14 : 0 (21 %), i-C15 : 0 (22·8 %) and ai-C15 : 0 (46·5 %) are the main cellular fatty acids; minor components are i-C14 : 0 (0·4 %), C15 : 0 (0·5 %), C16 : 0 (2·8 %), C16 : 1 (0·5 %), i-C17 : 0 (2·0 %), ai-C 17 : 0 (1·9 % %), C17 : 0 (0·15 %), i-C18 : 0 (1·1 %) and ai-C18 : 0 (0·1 %). Accumulates glycine betaine and glutamate as major osmoprotectants. Produces an exopolysaccharide when grown in minimal medium with trehalose. The following antibiotics (µg) inhibit growth: penicillin G (2), tetracycline (50), chloramphenicol (10), erythromycin (5), bacitracin (10), vancomycin (30), ampicillin (25), streptomycin (25), novobiocin (30) and lincomycin (15). Grows in the presence of kanamycin (30) and tetracycline (30). The G+C content of DNA of the type strain is 40·1 mol%. DNA–DNA relatedness of the type strain is 29·4 % with O. iheyensis DSM 1431T and 59 % with O. oncorhynchi NCIMB 14022T.
The type strain, strain 20AGT (=DSM 16557T=ATCC BAA-954T), was isolated from an algal mat collected from a sulfurous spring in the Santa Maria Incaldana site (Mondragone, Caserta Province, Campania, southern Italy).
Description of Oceanobacillus oncorhynchi subsp. oncorhynchi subsp. nov.
The creation of Oceanobacillus oncorhynchi subsp. incaldanensis automatically creates the subspecies Oceanobacillus oncorhynchi subsp. oncorhynchi. The description is the same as that given for Oceanobacillus oncorhynchi by Yumoto et al. (2005). The type strain is strain R-2T (=JCM 12661T=NCIMB 14022T).
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ACKNOWLEDGEMENTS |
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