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Istituto di Chimica Biomolecolare, Comprensorio ex Olivetti, via Campi Flegrei 34, 80078 Pozzuoli, NA, Italy
Correspondence
Assunta Giordano
agiordano{at}icmib.na.cnr.it
Agata Gambacorta
agambacorta{at}icmib.na.cnr.it
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ABSTRACT |
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Published online ahead of print on 15 July 2005 as DOI 10.1099/ijs.0.63864-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain 4AGT is AJ493661.
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; Nielsen et al., 1995). Alkaliphilic micro-organisms are also often halophilic. There are a large number of recognized species of the genus Bacillus and related genera that could be described as moderately halophilic or halotolerant, some of which are also alkaliphilic (Fritze, 1996; Nielsen et al., 1995; Romano et al., 2005; Yumoto et al., 2005). A number of approaches have been used to define this heterogeneous group taxonomically (Fritze, 1996, and references therein). Halophiles, slight halophiles, moderate halophiles, extreme halophiles halotolerants, alkaliphiles, alkalitolerants, etc., are classified in many genera (Amphibacillus, Bacillus, Gracilibacillus, Halobacillus, Marinococcus, Filobacillus, Halomonas, Oceanobacillus and Virgibacillus) (Arahal & Ventosa, 2002, and references therein). Jeon et al. (2005) proposed a novel genus, Alkalibacillus, based on a reclassification of [Bacillus] haloalkaliphilus as Alkalibacillus haloalkaliphilus and description of the novel species Alkalibacillus salilacus. In this study, a new halo-alkaliphilic strain, designated 4AGT, is characterized on the basis of a polyphasic approach. The strain was isolated from water samples collected from a mineral pool in Malvizza (Montecalvo Irpino, Avellino Province, Campania Region, southern Italy).
Strain 4AGT was isolated by the dilution-plating technique, from water (pH 8·0, 18 °C) taken from a small, bubbling pool in the resort of Montecalvo Irpino. The enrichment medium (medium 1) contained the following components (g l–1): Na2CO3, 3·0; KCl, 2·0; MgSO4.7H2O, 1·0; NaCl, 100; sodium citrate, 3·0; yeast extract, 10·0; MnCl2.4H2O, 0·36x10–3 and FeSO4, 50x10–3. Na2CO3 and NaCl were autoclaved separately. The pH of medium 1 was 9·0. Strain 4AGT was grown in medium containing 0–20 % (w/v) NaCl. The temperature range for growth was determined by incubating the isolate at 5–55 °C in medium 1. The pH dependence of growth was tested in the pH range 6·5–11·0 in medium 1 without Na2CO3. Growth on single carbon sources (medium 2) was tested on liquid media containing (g l–1): K2HPO4, 7·0; KH2PO4, 2·0; MgSO4.7H2O, 0·1; (NH4)2SO4, 1·0; NaCl, 100 and Na2CO3, 3·0; plus 500 µl l–1 of a thiamine hydrochloride solution (100 mg l–1) and the tested compounds (10·0 g l–1). Growth under anaerobic conditions at pH 7·5 and 9·0 was carried out in medium 1 in an anaerobic chamber for 5 days. In liquid medium, growth was followed by measuring OD540 and was scored as positive at values >0·250. Solid media were prepared by the addition of 1·8 % agar (w/v). A. haloalkaliphilus was grown according to the method described by Fritze (1996).
Cell morphology and spore formation were determined by using phase-contrast microscopy (Zeiss). Colony morphology was analysed on solid medium by using a Leica M8 stereomicroscope. All growth tests were performed at optimal growth temperatures for 3 days. Sensitivity of the strains to antibiotics was tested on medium 1 supplemented with 1·8 % (w/v) agar and Sensi-Discs (6 mm; Oxoid); incubation was for 48 h. The antibiotic tests were carried out according to the method of Romano et al. (1993). Casein and gelatin hydrolysis, oxidase, tyrosinase, L-aminopeptidase (Bactident-Merck) and catalase reactivities were tested in medium 1. Nitrate reduction was tested in medium 1 supplemented with 0·1 % (w/v) KNO3 (Jeon et al., 2005). Hydrolysis of hippurate was tested in medium 1 supplemented with 1 % (w/v) hippurate (Romano et al., 1996). Gram staining was performed according to the method of Dussault (1955). The KOH test was performed according to the method of Halebian et al. (1981). Hydrolysis of N'-benzoyl arginine-p-nitroaniline stereoisomers was tested by using the method of Oren & Galinski (1994). Extraction of intracellular solutes and their purification and quantification were conducted according to the methods of Romano et al. (2001).
Cell mass for quinone and lipid analysis was obtained from culture in medium 1 at 30 °C, pH 9·0 and at optimal NaCl concentration for growth. Lipid analysis was performed as reported by Romano et al. (2001). Lipid hydrolysis and identification of the fatty acid methyl esters were performed as reported by Romano et al. (2001). Quinones were analysed by liquid chromatography/mass spectroscopy (LC/MS) on a reversed-phase column, by electron ionization/mass spectroscopy (EI/MS) and 1H NMR spectra. Analyses of peptidoglycan structure and cell-wall sugars were carried out at the DSMZ according to the methods decsribed by Rhuland et al. (1955), Schleifer (1985), Schleifer & Kandler (1972) and Staneck & Roberts (1974). Total hydrolysis was was carried out by using 4 M HCl at 100 °C for 16 h and partial hydrolysis by using 4 M HCl at 100 °C for 45 min.
The DNA G+C content was determined by the method of Tamaoka & Komagata (1984); DNA was hydrolysed and the resultant nucleotides were analysed by HPLC (Mesbah et al., 1989).
DNA was isolated as described by Romano et al. (2003), and DNA–DNA hybridization was performed at the DSMZ with A. haloalkaliphilus WN13T. Hybridization was carried out spectroscopically as described by De Ley et al. (1970) with the modifications described by Huss et al. (1983) and Escara & Hutton (1980). Renaturation rates were computed with the TRANSFER.BAS program described by Jahnke (1992).
The total 16S rRNA gene sequence was determined by direct sequencing of the PCR-amplified 16S rRNA gene. Genomic DNA extraction, PCR-mediated 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 using an ABI Prism Dye Terminator cycle sequencing ready reaction kit (Applied Biosystems). Sequence reactions were electrophoresed by using an Applied Biosystems 373A DNA sequencer. For multiple sequence alignment, the program CLUSTAL W (Chenna et al., 2003) was used. 16S rRNA gene sequences for comparison were obtained from GenBank/EMBL or the RPD database. A phylogenetic tree based on 16S rRNA gene sequence comparisons (Fig. 1) was inferred by using the neighbour-joining method (Saitou & Nei, 1987) contained in the PHYLIP package, version 3.6 (Felsenstein, 2004). Evolutionary-distance matrices for the neighbour-joining method were calculated with the algorithm of Jukes & Cantor (1969) in the program DNADIST. Bootstrap analysis was performed with 1000 resamplings using SEQBOOT. A majority-rule (50 %) consensus tree was constructed for the topologies found by using CONSENSE (PHYLIP).
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; Schlesner et al., 2001). Colonies of strain 4AGT on enrichment medium 1 were usually white to transparent. Colonies were smooth, convex and regularly circular. The isolate required aerobic conditions for growth and grew in medium 1 containing 0–18 % NaCl, optimally at 10 %. Isolate 4AGT grew over a temperature range of 15–45 °C, optimally at 30 °C. The optimum pH for growth was 9·0 (pH range for growth was 7–10).
Strain 4AGT accumulated glycine betaine and glutamate under optimal growth conditions. It was able to grow in medium 2 containing glucose. Other carbon sources did not sustain growth. It was sensitive to vancomycin (30 µg), ampicillin (25 µg), novobiocin (30 µg), fusidic acid (10 µg), chloramphenicol (10 µg), erythromycin (5 and 30 µg), penicillin G (2 and 10 iu) and bacitracin (10 µg).
Strain 4AGT possessed complex lipids based on fatty acids. The total lipid content accounted for 9–11 % of the total dry weight of cells grown at the optimal growth conditions in medium 1 (pH 9·0, 10 % NaCl, 30 °C). Under these conditions, diphosphatidylglycerol (DPG) and phosphatidylglycerol (PG) were the main lipids (about 96 %), as identified by 1H and 13C NMR spectra. Chemical-shift values of signals present in these spectra were identical to those reported by Romano et al. (2001), with the exception of the absence of the signals due to double bonds in the fatty acid chains. Assignments were performed by comparison with commercial standards and by DEPT (distortionless enhancement by polarization transfer) experiments. Glycolipids were not detected. The fatty acid composition determined on cells grown under standard growth conditions was characterized by the abundance of branched, saturated acyl chains.
LC/MS and EI/MS analyses of the quinone content of strain 4AGT (about 0·1 % of the total dry weight of cells) indicated two characteristic major peaks corresponding to MK-7 and demethylmenaquinone with six repeating fully saturated isoprene units (DeMK-6), with a relative ratio of 7 : 3, respectively. The total hydrolysate of the peptidoglycan preparation contained the amino acids meso-diaminopimelic acid (meso-Dpm), alanine and glutamic acid. The partial hydrolysate of the peptidoglycan contained the peptides L-ala–D-glu and meso-dpm–D-Ala. These data indicate that the peptidoglycan type of strain 4AGT is A1
(meso-Dpm directly cross-linked) (DSMZ, 2001). Xylose was detected (trace amounts) as the only cell-wall sugar.
Strain 4AGT showed a high 16S rRNA gene sequence similarity (98·0 %) to A. haloalkaliphilus (Fritze, 1996), and the phylogenetic distance from any other recognized species within the genera Bacillus, Filobacillus, Halobacillus, Virgibacillus, Marinococcus and Oceonabacillus and from A. salilacus was <95·0 %.
The G+C content of the DNA of strain 4AGT was 39·5 mol%. DNA–DNA hybridization between strain 4AGT and DNA from A. haloalkaliphilus DSM 5271T (WN13T) indicated levels of DNA–DNA relatedness of 49·2 %. The assignment of strain 4AGT to a novel species, distinct from A. haloalkaliphilus, is clearly supported by both a low degree (49 %) of DNA–DNA relatedness (Rossellò-Mora & Amman, 2001; Stackebrandt & Goebel, 1994; Stackebrandt et al., 2002; Wayne et al., 1987) and by phenotypic differences (Table 1) from the two other recognized Alkalibacillus species (Fritze, 1996; Jeon et al., 2005).
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), but comprise the genera Halobacillus, Filobacillus, Marinococcus, Gracilibacillus, Oceanobacillus, Virgibacillus, Amphibacillus and Alkalibacillus (Arahal et al., 2000; Arahal & Ventosa, 2002; Hao et al., 1984; Heyrman et al., 2003; Jeon et al., 2005; Lu et al., 2001; Schlesner et al., 2001; Spring et al., 1996; Wainø et al., 1999; Yoon et al., 2004; Zhilina et al., 2001, and references therein).
Characteristics differentiating strain 4AGT from other Alkalibacillus species are summarized in Table 1. Cells of strain 4AGT were non-motile and the strain was less halophilic compared with related Alkalibacillus species. Strain 4AGT and A. haloalkaliphilus were able to hydrolyse gelatin, but did not reduce nitrate, in contrast to A. salilacus. Strain 4AGT and A. haloalkaliphilus were more alkaliphilic than A. salilacus. Strain 4AGT was the only strain tested that was oxidase-negative.
The quinone content of strain 4AGT and its closest relatives differed at the level of the minor components. The fatty acid profile of the three species was characterized by a large percentage of branched saturated fatty acids. In A. haloalkaliphilus, iso-C15 : 0 was most abundant, whereas in strain 4AGT iso-C17 : 0 and in A. salilacus, anteiso-C15 : 0 was present at a similar level to iso-C15 : 0.
Strain 4AGT formed a cluster with other Alkalibacillus species and represents a novel species, for which the name Alkalibacillus filiformis sp. nov. is proposed.
Description of Alkalibacillus filiformis sp. nov.
Alkalibacillus filiformis (fi.li.for'mis. L. neut. n. filum a thread; L. suff. -formis -like, of the shape of; N.L. masc. adj. filiformis thread-shaped).
Aerobic, alkalitolerant and halotolerant micro-organism of the phylum Firmicutes. Cells are Gram-positive, long, sporulating rods, 0·25–0·30 µm in width and 9·0–11·0 µm long. Spores are round-terminal. Colonies are white to transparent. Mesophilic, exhibiting optimum growth at 30 °C, but is able to grow between 15 and 45 °C and at pH 7·0–10·0 (optimal pH, 9·0). Tolerates up to 18 % NaCl [optimum growth at 10 % (w/v)]. Growth occurs in the absence of salt. Able to grow on glucose as sole carbon source. Gelatinase-positive, but negative for oxidase, casein, tyrosine, starch, hippurate and phenylalanine hydrolysis, and nitrate reduction. Catalase reaction is weak. Possesses 
-glucosidase activity. Menaquinones found are MK-7 (70 %) and DeMK-6 (30 %) and the predominant polar lipids are PG and DPG. Iso-C15 : 0, anteiso-C15 : 0, iso-C16 : 0, C16 : 0, iso-C17 : 0, anteiso-C17 : 0 are the main cellular fatty acids. The cell wall is type A1 (meso-Dpm directly cross-linked). Accumulates glycine betaine as a major component and glutamate as minor osmoprotectant. The DNA G+C content is 39·5 mol%. It is related phylogenetically to Alkalibacillus haloalkaliphilus on the basis of 16S rRNA gene sequence analysis, but shares only 49·2 % DNA–DNA relatedness with this species. Susceptible to the following antibiotics: chloramphenicol (10 µg), erythromycin (5 and 30 µg), penicillin G (2 and 10 iu), bacitracin (10 µg), vancomycin (30 µg), ampicillin (25 µg), fusidic acid (10 µg) and novobiocin (30 µg), but resistant to streptomycin (25 µg), tetracycline (30 and 50 µg), kanamycin (30 µg), neomycin (30 µg) and gentamicin (30 µg).
The type strain, 4AGT (=DSM 15448T=ATCC BAA-956T), was isolated from water of a small mineral pool with gas bubbles at the Malvizza site (Montecalvo Irpino, Campania Region, Italy).
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ACKNOWLEDGEMENTS |
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