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Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Sevilla, Sevilla, Spain
Correspondence
Encarnación Mellado
emellado{at}us.es
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Published online ahead of print on 22 April 2005 as DOI 10.1099/ijs.0.63560-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain G-19.1T is AJ717299.
Maximum-likelihood and maximum-parsimony trees are available as supplementary figures in IJSEM Online.
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). In this respect, the study of halophilic communities able to degrade aromatic compounds over a wide range of salinities is of great importance and will help in the characterization and identification of novel efficient pollutant-degrading micro-organisms.
Halophilic communities in saline and hypersaline environments are composed of species that fall mainly into two physiological groups, the extremely halophilic and the moderately halophilic bacteria and archaea (Ventosa et al., 1998), representing a promising ecosystem for biodegradation purposes. In recent years, efforts have been made to isolate halophilic bacteria able to degrade aromatic compounds (Margesin & Schinner, 2001; Mellado & Ventosa, 2003). However, little progress has been made in identifying the strains isolated. Of the moderately halophilic bacteria, a few members of the genera Halomonas, Marinobacter and Arhodomonas have been described as species able to degrade organic compounds (Adkins et al., 1993; Muñoz et al., 2001; Alva & Peyton, 2003; Nicholson & Fathepure, 2004; García et al., 2004; Huu et al., 1999; Hedlund et al., 2001). Less well known is the capacity of Gram-positive halophilic bacteria to degrade aromatic compounds, although other Gram-positive, non-halophilic genera are associated with degradation of these compounds, including both high-G+C Gram-positive bacteria, such as species of the genera Rhodococcus (Rast et al., 1980; Grund et al., 1992; Briglia et al., 1996; Eulberg et al., 1997; Yoon et al., 2000a, b), Arthrobacter (Eck & Belter, 1993; Westerberg et al., 2000) and Microbacterium (Arrault et al., 2002; Gauthier et al., 2003), and low-G+C Gram-positive bacteria, such as species of the genus Bacillus (Zhuang et al., 2002; Yumoto et al., 2003).
For a long time, the group formed by the moderately halophilic, Gram-positive, endospore-forming bacteria was very limited and most of these micro-organisms were assigned to the genus Bacillus (Slepecky & Hemphill, 1991). However, in recent years a number of novel genera and species have been described, such as the genus Halobacillus, which accommodates six species. This genus includes Gram-positive, spore-forming, moderately halophilic, motile bacteria possessing peptidoglycan of the Orn–D-Asp type. The type species of the genus is Halobacillus halophilus, previously described as Sporosarcina halophila (Claus et al., 1983; Ventosa et al., 1983); the other Halobacillus species are Halobacillus trueperi, H. litoralis (Spring et al., 1996), H. karajensis (Amoozegar et al., 2003), H. salinus (Yoon et al., 2003) and H. locisalis (Yoon et al., 2004). In addition to species belonging to the genus Halobacillus, other spore-forming and halophilic species are found within the genera Virgibacillus (Heyndrickx et al., 1999; Heyrman et al., 2003), Gracilibacillus (Wainø et al., 1999), Filobacillus (Schlesner et al., 2001), Jeotgalibacillus (Yoon et al., 2001), Lentibacillus (Yoon et al., 2002; Namwong et al., 2005; Jeon et al., 2005), Pontibacillus (Lim et al., 2005a, b) and Tenuibacillus (Ren & Zhou, 2005).
Recently, we characterized an active and acclimatized bacterial population able to degrade aromatic compounds in saline habitats in southern Spain. In this study, we isolated several strains that represented the dominant, culturable, moderately halophilic bacteria by using an enrichment culture method previously used for phenol and p-coumaric acid (García et al., 2004). For the enrichment strategy, cultures of sterile modified mineral medium M63 [KOH, 0·075 M; KH2PO4, 0·1 M; (NH4)2SO4, 0·015 M; 1 % (v/v) MgSO4/FeSO4 solution (MgSO4, 1·6 mM; FeSO4, 39 µM)] (Cohen & Rickenberg, 1956) supplemented with 10 % NaCl and 0·005 % yeast extract were used. Phenol was added to this medium at a concentration of 0·05 % (w/v). Enrichments were incubated at 37 °C in a shaker incubator at 200 r.p.m. After 4 days incubation, 1 ml enrichment was transferred into fresh medium and the medium was reincubated. Bacterial growth was monitored by observing increasing turbidity of the medium. After three successive transfers, the enriched cultures were plated on a solid version (18 g agar l–1) of modified M63 medium and incubated at 37 °C. A negative control containing no substrate was also included. Each individual colony was again checked for its ability to grow on phenol, after inoculation in the liquid selective medium described previously.
The enrichment procedure selected a limited number of fast-growing, phenol-degrading bacteria, which were mainly Gram-negative. However, a Gram-positive, rod-shaped strain, G-19.1T, showing a high level of degradative activity was isolated. The aim of the present study is to unravel the taxonomic and phylogenetic status of G-19.1T, using a combination of phenotypic and phylogenetic analyses. To our knowledge, this is the first Gram-positive, moderately halophilic, phenol-degrading bacterium to be subjected to phylogenetic analysis.
The isolate was routinely grown on a complex saline medium (SW) with a final concentration of 10 % (w/v) total salts (SW-10) supplemented with 0·5 % (w/v) yeast extract (Nieto et al., 1989). The strain was cultivated at 37 °C in an orbital shaker (New Brunswick Scientific) at 200 r.p.m. When necessary, solid medium was prepared by adding 20 g Bacto agar l–1 (Difco).
Strain G-19.1T was examined for a range of phenotypic properties using standard procedures (Ventosa et al., 1982; Quesada et al., 1984; García et al., 1987). Cells of strain G-19.1T were found to be Gram-positive rods that were oxidase-negative, catalase-positive and strictly aerobic. On SW-10 medium incubated at 37 °C for 48 h, the strain produced cream-coloured, circular, convex and uniformly round colonies with a diameter of 1–2 mm. Ellipsoidal endospores were observed in a central position. No pigment was produced in the medium. Most species of the genus Halobacillus are characterized by their orange-pigmented colonies (Spring et al., 1996; Yoon et al., 2003, 2004). In contrast to species of Halobacillus, strain G-19.1T does not produce orange colonies, is negative for oxidase and is able to reduce nitrate to nitrite. Several other features that distinguish strain G-19.1T from its close phylogenetic relatives are shown in Table 1.
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The nutritional features of G-19.1T were determined by using GP MicroPlates (Biolog). Strains were grown on isolate medium (Biolog) at 37 °C for 24 h. Suspensions of the strains were made using sterile saline medium (3 % NaCl). Immediately after the cells had been suspended in the saline solution, Biolog GP MicroPlates were inoculated and incubated at 37 °C for 24 h. The results were read with a MicroPlate Reader using MICROLOG 3.59 computer software to perform automated reading. The results of the nutritional tests are given in the species description.
Genomic DNA was prepared using the method described by Marmur (1961). A PCR was carried out for the amplification of the almost-complete 16S rRNA gene (1506 bp) by using primers 16F27 and 16R1488 (Mellado et al., 1995). Sequencing was performed using an automated DNA sequencer (model 3100; Applied Biosystems). The DNA sequences were analysed using the ARB software package (Ludwig & Strunk, 1996). The 16S rRNA gene sequences were aligned and the alignment confirmed and checked against both primary and secondary structure of the 16S rRNA molecule by using the alignment tool of the ARB software package. The aligned sequences were subjected to different phylogenetic methods integrated into the ARB software for phylogenetic inference. These methods included maximum-likelihood (Felsenstein, 1981), maximum-parsimony (Kluge & Farris, 1969) and neighbour-joining (Saitou & Nei, 1987) procedures. Base-frequency filters were applied in the sequence comparison analysis and the effects on the results evaluated.
A comparison using 16S rRNA gene sequences available in the databases revealed that the 16S rRNA gene sequence of strain G-19.1T displays a high level of similarity to those from Halobacillus species with validly published names (96·2–97·0 % sequence similarity). Other spore-forming and halophilic or halotolerant taxa (Virgibacillus, Gracilibacillus, Lentibacillus and Pontibacillus species, Filobacillus milensis, Bacillus haloalkaliphilus and Tenuibacillus multivorans) were more distantly related to strain G-19.1T, displaying 16S rRNA gene sequence similarity below 95 %.
In the tree based on the neighbour-joining algorithm (Saitou & Nei, 1987), strain G-19.1T falls within the radiation of the cluster comprising members of the genus Halobacillus, but emerges as a separate entity. These results are congruent with those obtained using the maximum-likelihood and maximum-parsimony algorithms. The neighbour-joining tree in Fig. 1 shows the relationship between strain G-19.1T and the other species of the genus Halobacillus and other related bacteria. Maximum-likelihood and maximum-parsimony trees are available as supplementary figures in IJSEM Online.
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, described in detail in Mormile et al. (1999). The levels of DNA–DNA hybridization between strain G-19.1T and the phylogenetically related Halobacillus species were low and, in any case, below 70 % (H. trueperi DSM 10404T, 32 %; H. litoralis DSM 10405T, 13 %; H. salinus KCCM 41590T, 31 %; H. karajensis DSM 14948T, 25 %), providing decisive evidence that strain G-19.1T is not genotypically related to the Halobacillus species tested.
The G+C content of the genomic DNA, determined by using the method of Marmur & Doty (1962) with the equation of Owen & Hill (1979), was 42·4 mol%.
The cell-wall peptidoglycan was analysed according to Schleifer & Kandler (1972) by the Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH (DSMZ, Braunschweig, Germany). The analysis showed that strain G-19.1T possessed peptidoglycan type A1
with m-diaminopimelic acid (m-Dpm) as the diagnostic diamino acid. The major isoprenoid quinone was MK-7. The cellular fatty acids of strain G-19.1T were analysed with the MIDI system (Microbial ID). Cells were cultured in SW-7.5 medium (Ventosa et al., 1982) at 37 °C for 24 h. The predominant fatty acids of strain G-19.1T were anteiso-C15 : 0 (52·3 %), iso-C16 : 0 (10·5 %), iso-C15 : 0 (10·2 %), anteiso-C17 : 0 (8·3 %), anteiso-C17 : 1 (5·1 %) and iso-C14 : 0 (4·8 %). Strain G-19.1T and the phylogenetically related genera contained similar fatty acid profiles, having anteiso-C15 : 0 as a major fatty acid (Table 1
).
Overall, our results showed that strain G-19.1T exhibited the closest phylogenetic affiliation to Halobacillus species; however, comparative 16S rRNA gene sequence analysis showed that this strain represents a novel branch within the category of Gram-positive spore-forming rods. A cell-wall type based on Orn–D-Asp constitutes a key characteristic that differentiates members of the genus Halobacillus from other phylogenetically related genera of endospore-forming rods (Arahal & Ventosa, 2000). The results obtained in our chemotaxonomic analysis, revealing a cell-wall type based on m-Dpm, support the conclusion that strain G-19.1T cannot be assigned to the genus Halobacillus. In addition, some phenotypic features differentiate isolate G-19.1T from species of Halobacillus (Table 1), a genus that was defined as being oxidase-positive and unable to reduce nitrate to nitrite (Spring et al., 1996), two features that differ from those of strain G-19.1T.
Strain G-19.1T was phylogenetically related at a 16S rRNA gene sequence similarity level below 95 % to other genera with a cell-wall type based on m-Dpm. In addition, some chemotaxonomic and phenotypic features differentiate isolate G-19.1T from phylogenetically related spore-forming taxa (Table 1). Strain G-19.1T is oxidase-negative, whereas other related m-Dpm-containing genera, such as Gracilibacillus and Tenuibacillus, are described as being oxidase-positive. The genus Filobacillus is defined as being oxidase-negative, like strain G-19.1T; however, this genus does not reduce nitrate to nitrite, a characteristic that is useful for differentiating it from strain G-19.1T. Members of other related m-Dpm-containing genera such as Gracilibacillus, Virgibacillus and Tenuibacillus hydrolyse aesculin, unlike strain G-19.1T.
Overall, the phenotypic, genotypic and phylogenetic analyses performed suggested that strain G-19.1T cannot be assigned to any known taxon. We therefore propose to classify this novel isolate in a novel genus and species separate from all m-Dpm-containing bacilli as well as the genus Halobacillus, for which the name Thalassobacillus devorans gen. nov., sp. nov. is proposed.
Description of Thalassobacillus gen. nov.
Thalassobacillus (Tha.las'so.ba.cil'lus. Gr. fem. n. thalassa sea; L. masc. n. bacillus rod; N.L. masc. n. Thalassobacillus rod from the sea).
Gram-positive, spore-forming, rod-shaped cells. Motile. Catalase-positive, oxidase-negative and urease-negative. Nitrate is reduced to nitrite. Ellipsoidal endospores in central position. Moderately halophilic: does not grow in media without NaCl. Cell-wall peptidoglycan type A1 with m-Dpm. Major fatty acids are anteiso-C15 : 0, iso-C16 : 0 and iso-C15 : 0. Predominant menaquinone is MK-7. The G+C content of the DNA of the type species is 42·4 mol%. The type species is Thalassobacillus devorans.
Description of Thalassobacillus devorans sp. nov.
Thalassobacillus devorans [de.vo'rans. L. v. devorare to devour; L. part. adj. devorans devouring (organic compounds)].
Cells are 2·0–4·0x1·0–1·2 µm. Motile by means of flagella. Colonies are uniformly round, circular, regular, convex and cream-coloured on SW-10 medium. Moderately halophilic, growing in a wide range (0·5–20 %, w/v) of salt concentrations, with optimum growth at 7·5–10 % (w/v) salts. No growth in the absence of NaCl. No other salt requirements determined. Growth occurs at 15–45 °C (optimal temperature 37 °C) and at pH 6·0–10·0 (optimal pH is 7·0). Strictly aerobic. Aesculin is not hydrolysed. Indole, methyl red and Voges–Proskauer tests are negative. Gelatin and Tween 80 are hydrolysed. Starch and casein are not hydrolysed. Acid is produced from D-glucose, D-trehalose, D-mannose and D-fructose. As determined by the Biolog GP panel, the following compounds are utilized: dextrin, N-acetyl-D-glucosamine, N-acetyl-D-mannosamine, D-fructose, 
-D-glucose, maltose, maltotriose, D-mannitol, D-mannose, D-melezitose, 3-methyl glucose, palatinose, D-psicose, D-sorbitol, sucrose, D-trehalose, acetic acid, 
-hydroxybutyric acid, -ketovaleric acid, pyruvic acid, thymidine and uridine. The following compounds are not utilized as sole carbon and energy sources (Biolog): -cyclodextrin, -cyclodextrin, glycogen, inulin, mannan, Tweens 40 and 80, amygdalin, L-arabinose, D-arabitol, arbutin, cellobiose, L-fucose, D-galactose, D-galacturonic acid, gentiobiose, D-gluconic acid, myo-inositol, -D-lactose, lactulose, D-melibiose, methyl -D-galactoside, methyl -D-galactoside, methyl -D-glucoside, methyl -D-glucoside, methyl -D-mannoside, D-raffinose, L-rhamnose, D-ribose, salicin, sedoheptulosan, stachyose, D-tagatose, turanose, xylitol, D-xylose, -hydroxybutyric acid, -hydroxybutyric acid, p-hydroxyphenylacetic acid, -ketoglutaric acid, lactamide, D-lactic acid methyl ester, L-lactic acid, D-malic acid, L-malic acid, methyl pyruvate, monomethyl succinate, propionic acid, succinamic acid, succinic acid, N-acetyl-L-glutamic acid, alaninamide, D-alanine, L-alanine, L-alanyl glycine, L-asparagine, L-glutamic acid, glycyl L-glutamic acid, L-pyroglutamic acid, L-serine, putrescine, 2,3-butanediol, glycerol, adenosine, 2'-deoxyadenosine, inosine, adenosine 5'-monophosphate, thymidine 5'-monophosphate, uridine 5'-monophosphate, fructose 6-phosphate, glucose 1-phosphate, glucose 6-phosphate and -DL-glycerol phosphate. Other characteristics as for the genus. The DNA G+C content of the type strain is 42·4 mol%.
The type strain, G-19.1T (=DSM 16966T=CECT 7046T=CCM 7282T), was isolated from a saline soil in southern Spain.
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ACKNOWLEDGEMENTS |
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