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Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Seville, Spain
Correspondence
Antonio Ventosa
ventosa{at}us.es
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain G-16.1T is AJ616910.
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). Moreover, extremophiles in this group exhibit great potential for biotechnological exploitation: in fact, these bacteria have been used as a source of compatible solutes or hydrolytic enzymes (Mellado & Ventosa, 2003).
Saline and hypersaline environments are often contaminated with organic compounds as a result of industrial activities and urban water effluents. Although the use of different bacterial groups in bioremediation processes has been widely studied, the ability of native communities of halophilic bacteria to be used for the degradation of pollutants in saline habitats has not been studied in a systematic way, and only a few studies have reported the biotechnological potential of this group of extremophiles in the decontamination of saline environments (Margesin & Schinner, 2001; Mellado & Ventosa, 2003). Thus, the identification of moderate halophiles that play an important role in the degradation of pollutant compounds is of great interest in the context of assessing acceleration of the environmental repair process for bioremediation in contaminated saline habitats.
Recently, we have focused on the characterization of the moderately halophilic bacterial community able to degrade different aromatic pollutants in saline habitats of southern Spain, the primary goal being the isolation of potential degraders able to grow at different salinities. In the course of this work, four novel bacterial strains, designated G-16.1T, G-2.5, G-17.1 and H-30.2, were isolated from saline soils in Isla Cristina (Huelva), Spain. These bacteria were isolated because of their ability to grow in phenol (strains G-16.1T, G-2.5, G-17.1) or p-coumaric acid (strain H-30.2) as the sole source of carbon and energy. For this purpose, an enrichment culture using sterile mineral medium M63 (Cohen & Rickenberg, 1956) supplemented with 10 % NaCl was used. Phenol or p-coumaric acid was added to the mineral medium at a concentration of 0·05 % (w/v). After three enrichment steps, the cultures obtained were plated on M63+10 % NaCl medium supplemented with the organic compound and incubated at 37 °C. Colonies that differed in appearance from each other were picked and inoculated into the liquid selective medium previously described. Of the isolates, four strains showing a high level of degradative activity were selected for further studies.
To study the ability of the isolates to degrade a variety of aromatic compounds, substrates were added to the saline minimal medium M63+10 % NaCl at different concentrations (0·05 % for phenol and p-coumaric acid and 1–5 mM for the other substrates). This medium was inoculated with strains G-16.1T, G-2.5, G-17.1 and H-30.2, and the utilization of these compounds was tested by monitoring the increase in turbidity. This group of isolates utilized, in addition to phenol and p-coumaric acid, a diverse range of compounds as sole carbon and energy sources (Table 1), indicating that they constitute promising potential degraders in bioremediation processes. The aim of this work was to study these four isolates in detail by using a polyphasic taxonomic approach.
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with a single species, Halomonas elongata. Currently, the genus comprises more than 20 species, including bacterial isolates from different terrestrial and aquatic environments with, in most cases, high salt concentrations. This genus has been considered as a model system among the moderate halophiles and has been used extensively for studies concerning both osmoregulatory mechanisms and physiological adaptations (Ventosa et al., 1998; Nieto et al., 2000). On the other hand, the genus Halomonas is a taxon comprising strains that are metabolically versatile: some Halomonas species have been described as denitrifying halophilic bacteria useful in the reduction of nitrate during the treatment of saline waste (Berendes et al., 1996; Mormile et al., 1999; Romano et al., 1996; Dobson & Franzmann, 1996). In addition, there are also a few reports on Halomonas strains able to degrade aromatic pollutants (Maltseva et al., 1996; Muñoz et al., 2001).
The isolates were cultured on a complex medium (SW-10) containing 10 % salts supplemented with 0·5 % (w/v) yeast extract (Ventosa et al., 1982). The strains were routinely grown at 200 r.p.m. in an orbital shaker (New Brunswick Scientific) at 37 °C. When necessary, solid medium was prepared by adding 20 g Bacto-agar l–1 (Difco).
The methods used for phenotypic characterization have been described previously in detail (Ventosa et al., 1982; Quesada et al., 1984; García et al., 1987). Isolates G-16.1T, G-2.5, G-17.1 and H-30.2 were Gram-negative rods that were oxidase-negative, catalase-positive and strictly aerobic. On SW-10 medium incubated at 37 °C, the strains produced circular colonies, each 2–3 mm in diameter. Colonies were flat/slightly convex with irregular edges.
The salt requirement of these strains was determined in complex medium SW at different salt concentrations. The isolates grew in a wide range of salinities (from 1·5 to 30 %, w/v, salt), producing optimal growth in media containing 7·5–10 % (w/v) salt. They did not grow in the absence of NaCl. These results indicated that the four isolates were strictly halophilic and could be assigned to the group of moderately halophilic bacteria (Kushner & Kamekura, 1988). Some other physiological characteristics of the strains are shown in Table 2 and in the species description.
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Chromosomal DNA from the four strains was isolated and purified according to the methods described by Wilson (1987) and Marmur (1961). The 16S rRNA genes of the four isolates were amplified by a PCR using two universal primers, as described previously (Mellado et al., 1995), and almost-complete nucleotide sequences (approx. 1450 bp) were determined. The ARB software package (Ludwig & Strunk, 1996) was used for 16S rRNA gene sequence analysis.
16S rRNA gene phylogenetic analysis performed on the basis of the neighbour-joining method (Saitou & Nei, 1987) clearly showed the position of this group of strains within the family Halomonadaceae, in the genus Halomonas. Maximum-parsimony- and maximum-likelihood-based trees using the full dataset or a selection of sequences were also obtained which showed the same phylogenetic position of the group of isolates, i.e. in the genus Halomonas, grouped together and forming a cluster separate from the other species (Fig. 1). Base-frequency filters were applied in the sequence comparison analysis and the effects on the results were evaluated.
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The similarities between the 16S rRNA gene nucleotide sequences of the isolates and those of the other 25 currently accepted Halomonas species were between 93 and 98 %. The highest similarity values between the sequence of strain G-16.1T and those of the type strains of species of the genus were for Halomonas salina (98·0 %) and Halomonas halophila (98·0 %). These two species have 99·0 % 16S rRNA gene sequence similarity but are considered different species on the basis of other phenotypic and genotypic data (Valderrama et al., 1991).
Recently, Arahal et al. (2002) performed a phylogenetic analysis of the genus Halomonas based on 23S and 16S rRNA gene sequence comparisons: two clear phylogenetic groups were observed. Group 1 comprises the type species of Halomonas, H. elongata and four other species, Halomonas eurihalina, Halomonas halmophila, H. halophila and H. salina. Since the publication of this work, a number of novel species belonging to the genus Halomonas have been described, and our phylogenetic analysis based on the sequence of 16S rRNA genes reveals that Halomonas maura could also be included in group 1. The phylogenetic analyses performed also show that strains G-16.1T, G-2.5, G-17.1 and H-30.2 cluster with species belonging to the above-mentioned Halomonas group 1 (Fig. 1
) and show clearly that they are members of the Halomonas ‘sensu stricto group’.
The G+C content of genomic DNA was determined by the method of Marmur & Doty (1962) using the equation of Owen & Hill (1979): the values for our isolates ranged between 61·0 and 62·9 mol%. These values fall within the range described for species of the genus Halomonas (52–68 mol%; Franzmann et al., 1988). However, the G+C content is lower than those of the most phylogenetically related species (64·2 mol% for H. salina, 66·7 mol% for H. halophila).
To define the taxonomic position of the novel isolates able to degrade different organic pollutants, DNA–DNA hybridization studies were carried out according to the competition procedure of Johnson (1994), described in detail in Mormile et al. (1999). The hybridization temperature was 57 °C, which is within the limit of validity for the filter method (De Ley & Tijtgat, 1970), and the percentage of hybridization was calculated according to Johnson (1994). The values obtained in the DNA–DNA hybridization studies between strain G-16.1T and the type strains of the Halomonas species with which it formed a phylogenetically coherent cluster are shown in Table 3. The DNA–DNA hybridization between strain G-16.1T and isolates G-2.5, G-17.1 and H-30.2 was equal to, or greater than, 90 %, confirming the phylogenetic data and the phenotypic characteristics shared by this group of strains. On the other hand, DNA–DNA hybridization between strain G-16.1T and closely related species of the genus Halomonas was significantly below 70 %, showing relatedness values of 49 % with H. salina and 11 % with H. halophila, indicating that this strain is genotypically distinct from the type strains of these species (Wayne et al., 1987).
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. Overall, the phenotypic, genotypic and phylogenetic results suggest that isolates G-16.1T, G-2.5, G-17.1 and H-30.2 should be assigned to a novel species within the genus Halomonas. On the basis of the ability of these isolates to degrade different aromatic organic compounds, the name Halomonas organivorans sp. nov. is proposed.
Description of Halomonas organivorans sp. nov.
Halomonas organivorans (N.L. n. organum organic compound; L. v. vorare to eat, to consume; N.L. part. adj. organivorans devouring organic compounds).
Cells are motile, Gram-negative rods, 2·0–3·0x1·0–1·2 µm. Colonies are cream, flat/slightly convex, opaque and raised with slightly irregular edges on SW-10 medium. Moderately halophilic, growing in a wide range (1·5–30 %, 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 have been determined. Growth occurs at 15–45 °C (optimal temperature 37 °C) and at pH 6·0–10·0 (optimal pH 7·0). Strictly aerobic. Catalase is produced, aesculin is hydrolysed. Negative results in oxidase, indole, methyl red and Voges–Proskauer tests. Gelatin, casein, starch and DNA are not hydrolysed. As determined with the Biolog GN panel, the following compounds are utilized: glycogen, Tween 40, Tween 80, N-acetyl-D-glucosamine, D-arabitol, i-erythritol, D-fructose, D-galactose, 
-D-glucose, m-inositol, D-mannitol, D-mannose, D-psicose, L-rhamnose, D-sorbitol, sucrose, D-trehalose, methylpyruvate, monomethyl succinate, acetic acid, cis-aconitic acid, citric acid, D-galactonic acid lactone, D-galacturonic acid, D-glucuronic acid, D-gluconic acid, 
-hydroxybutyric acid, p-hydroxyphenylacetic acid, -ketoglutaric acid, DL-lactic acid, malonic acid, D-saccharic acid, succinic acid, bromosuccinic acid, D-alanine, L-alanine, L-alanyl-glycine, L-asparagine, L-aspartic acid, L-glutamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-proline, L-serine, L-threonine, urocanic acid, inosine, uridine, putrescine, 2-aminoethanol and glycerol. The following compounds are not utilized: -cyclodextrin, dextrin, N-acetyl-D-galactosamine, adonitol, L-arabinose, cellobiose, L-fucose, gentiobiose, -D-lactose, lactulose, maltose, D-melibiose, methyl -D-glucoside, D-raffinose, turanose, xylitol, formic acid, D-glucosaminic acid, -hydroxybutyric acid, 
-hydroxybutyric acid, itaconic acid, -ketobutyric acid, -ketovaleric acid, propionic acid, quinic acid, sebacic acid, succinamic acid, glucuronamide, alaninamide, glycyl-L-aspartic acid, glycyl-L-glutamic acid, L-ornithine, L-phenylalanine, L-pyroglutamic acid, D-serine, DL-carnitine, -aminobutyric acid, thymidine, phenylethylamine, 2,3-butanediol, DL--glycerol phosphate, D-glucose 1-phosphate and D-glucose 6-phosphate. The DNA G+C content ranges between 61·0 and 62·9 mol%.
Isolated from saline soils. The type strain is G-16.1T (=CECT 5995T=CCM 7142T). The DNA G+C content of the type strain is 61·0 mol%. One important property of this strain is its ability to utilize various organic compounds (Table 1) considered as pollutants as sole sources of carbon and energy.
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ACKNOWLEDGEMENTS |
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