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Department of Civil and Environmental Engineering, University of California, Berkeley, CA 94720-1710, USA
Correspondence
Lisa Alvarez-Cohen
alvarez{at}ce.berkeley.edu
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ABSTRACT |
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, meso-diaminopimelic acid. The major menaquinone is MK-8 (H4). Mycolic acids are absent. The G+C content is 74 mol%. Based on morphological, physiological, chemotaxonomic and phylogenetic evidence, it is proposed that strain CB1190T (=ATCC 55486T=DSM 44775T) be classified as the type strain of a novel species, Pseudonocardia dioxanivorans sp. nov. Further studies with this organism will provide insights into metabolic pathways, responsible enzymes, kinetics and the fate of 1,4-dioxane in the environment.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of Pseudonocardia dioxanivorans CB1190T is AY340622.
A scanning electron micrograph of cells of strain CB1190T and details of fatty acid compositions are available as supplementary material in IJSEM Online.
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), chlorinated solvents (Wackett et al., 1989), explosives (Pasti-Grigsby et al., 1996), plasticizers (Klausmeier & Osman, 1976) and azo dyes (Zhou & Zimmermann, 1993). Within the actinomycetes, members of the genus Pseudonocardia (Henssen, 1957; Huang et al., 2002) have been reported to use hydrocarbons (Juteau et al., 1999; Lechevalier et al., 1986; Lee et al., 2004), methyl sulfides (Reichert et al., 1998) and tetrahydrofuran (THF) (Kohlweyer et al., 2000) as growth substrates.
In this paper, we describe a novel Pseudonocardia species that is the only known pure culture that can grow on 1,4-dioxane, a toxic groundwater pollutant (Parales et al., 1994). This culture can be used for bioaugmentation at 1,4-dioxane- and THF-contaminated sites. 1,4-Dioxane is widely used as a stabilizer for chlorinated compounds and as a solvent in the manufacture of textiles, organic chemicals, fumigants, automotive coolants and hygiene products (Mohr, 2001). 1,4-Dioxane is a probable human carcinogen and a priority pollutant that has been detected in surface and ground waters (Mohr, 2001).
The culture CB1190 was graciously supplied by Dr Rebecca Parales, University of California, Davis. It was originally enriched by Parales and co-workers from 1,4-dioxane-contaminated industrial sludge from Darlington, SC, USA (Parales et al., 1994). The initial enrichments were performed in basal salts medium with 1·5–4·0 mM THF in the presence of 0·1 % (w/v) yeast extract. Enrichments capable of degrading both 1,4-dioxane and THF were selected. The mixed enrichment degraded up to 10 mM 1,4-dioxane per day. Only one prokaryotic isolate, designated strain CB1190T, was capable of growing on 1,4-dioxane as sole carbon source.
In our laboratory, CB1190T was grown aerobically in ammonium mineral salts (AMS) liquid medium (Parales et al., 1994) at 30 °C with 5 mM 1,4-dioxane. Cell biomass was quantified as total protein concentration (Lontoh & Semrau, 1998). BSA was used as a standard for the Coomassie Plus protein assay kit (Pierce). Cells of strain CB1190T were also maintained on plates containing AMS and 1·5 % Bacto agar. The plates were incubated at 30 °C in a desiccator in which 1,4-dioxane was supplied in the vapour phase by placing a glass microfibre filter (Whatman) in the bottom half of a glass Petri dish placed on the floor of the desiccator. An aliquot of 250 µl 1,4-dioxane that had been filter-sterilized (0·1 µm pore size) was added to the filter. Every 4–5 days, the filters were replaced with new dioxane-laden filters in the fume hood. The colours and shapes of colonies were recorded weekly. A Hitachi model S-5000 microscope was used for scanning electron microscopy of gold-coated, dehydrated cells. Fourteen-day-old cultures on AMS-agar plates were visualized by electron microscopy.
The ability of CB1190T and reference strains Pseudonocardia hydrocarbonoxydans DSM 43281T and Pseudonocardia sulfidoxydans DSM 44248T to grow aerobically on a variety of carbon sources was investigated using GP2 and SFP2 microplates (Biolog). Cells were grown at 30 °C on Biolog universal growth agar amended with 0·25 % glucose. The OD590 of the inoculum was adjusted to 0·2 before loading 150 µl into each well. Similarly, the utilization of various nitrogen sources was tested using the Biolog PM3 microplate. For PM3 plates, the OD590 of the inoculum was adjusted to 0·4 before loading 100 µl into each well. The wells were analysed using the Omnilog system after incubating the plates for 7 days at 30 °C. In addition, the capability of P. sulfidoxydans and P. hydrocarbonoxydans to grow on THF and 1,4-dioxane was tested. The ability of CB1190T to grow on 1,4-dioxane (99·8 % pure; Aldrich Chemical) and Luria–Bertani (LB) broth (Becton Dickinson) under anaerobic conditions was investigated. The temperature range for growth was examined. Standard phenotypic tests commonly used for describing novel species of actinomycetes were performed (Gordon et al., 1974). The cells were grown in AMS medium with 1,4-dioxane added as the sole carbon source and incubated at 30 °C for up to 28 days. The pH of AMS medium was adjusted to 7·0 for examining acid production from various carbohydrates, which were added to the AMS medium to achieve 1 % (w/v) aqueous concentration.
For monitoring growth on 1,4-dioxane, liquid samples were collected at various intervals and filtered with 0·45 µm syringe filters to eliminate cells. Dioxane disappearance was measured by injecting 5 µl filtered liquid samples into a Varian 3400 gas chromatograph equipped with a flame-ionization detector (FID) and a GraphPac-GB column (Alltech). The injector, oven and detector temperatures were respectively set at 220, 150 and 250 °C. Cell growth was determined by measuring total protein and enzymic activities of soluble monooxgenases were assayed as described by Brusseau et al. (1990). Briefly, duplicate 5-ml aliquots of CB1190T cell suspensions were transferred to 20 ml glass serum vials containing approximately 5 mg crystalline naphthalene. The vials were sealed with Teflon-lined rubber septa and incubated at 30 °C on a platform shaker for 15 min. Fifty microlitres of freshly prepared 5 mg tetrazotized o-dianisidine ml–1 were added to the samples. Naphthalene was oxidized to a mixture of 1-naphthol and 2-naphthol by the monooxygenase. The naphthols were detected colorimetrically by reaction with tetrazotized o-dianisidine to form purple diazo dyes.
The capability of strains to fix dinitrogen was tested by the activity of nitrogenase, which converts acetylene into ethylene in the presence of an external energy source (Chu & Alvarez-Cohen, 1996). Briefly, 1 ml acetylene and 20 mM glucose were added to 5 ml cell culture in nitrogen-free AMS medium. The vials were incubated at 30 °C on a shaker at 150 r.p.m. The headspace concentrations of acetylene and ethylene were analysed by an HP 5890 series II gas chromatograph equipped with an FID. Acetylene-free controls were used to determine background ethylene production. Stoichiometric decrease in acetylene concentration with concomitant production of ethylene was indicative of nitrogenase activity. Ammonia produced by nitrogen-fixing cells was assayed using the Nessler method (Hach method 8038). The colour produced by the reaction of Nessler reagent and ammonium ions was measured at 425 nm using a Hach DR/2500 spectrophotometer. Uninoculated N-free AMS medium was used as a blank for the colorimetric assay.
Whole-cell fatty acid methyl ester (FAME) analysis was performed by Microchek, Inc. (Northfield, VT, USA) using gas chromatography. The cells were grown at 30 °C on BBL trypticase soy broth (BD Diagnostic Systems) for 7 days prior to FAME analysis. Phospholipid fatty acid (PLFA) analysis was performed on 14-day-old cultures grown in AMS and 5 mM 1,4-dioxane at 30 °C. The cells were saponified, methylated, solvent-extracted and analysed by GC-MS by using the modified Bligh/Dyer method (White & Ringelberg, 1998). Analysis of quinones and mycolic acids was carried out by the Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH (DSMZ), Braunschweig, Germany. The diagnostic diamino acid was determined by analysis of a whole-cell hydrolysate by TLC on cellulose (Hasegawa et al., 1983; Rhuland et al., 1955). Gram staining was performed according to the standard method (Gerhardt et al., 1994).
Genomic DNA was extracted from CB1190T by a two-step enzymic treatment followed by bead-beating lysis and organic extraction (Dojka et al., 1998). PCR amplification of the 16S rRNA gene using bacterial primers 8F (5'-AGAGTTTGATCCTGCCTCAG-3'), 338F (5'-CCTACGGGAGGCAGCAG-3') and 1492R (5'GGYTACCTTGTTACGACTT-3') was carried out as described by Richardson et al. (2002). Purified PCR products were directly sequenced using an Applied Biosystems 3100 Genetic Analyzer at the University of California Berkeley Sequencing Facility. The partial sequences were aligned using the Autoassembler program version 2.1 (PE Biosystems). CHECK_CHIMERA software (http://rdp.cme.msu.edu/) was used to confirm that the sequences were not of chimeric origin. The 16S rRNA gene sequences were compared with those in the GenBank database using the BLAST program (http://www.ncbi.nlm.nih.gov/blast). Detailed phylogenetic analyses were carried out using the ARB program (http://www.arb-home.de). Evolutionary distance dendrograms were constructed using the Felsenstein substitution model and neighbour-joining tree-building algorithm. Since all input sequences were longer than 1250 bp, the parsimony tool was not used. Statistical support for branch points in the dendrograms was estimated by bootstrap resampling analysis of 1000 independent trees (Felsenstein, 1985) using PAUP 4.0 program.
DNA base composition (G+C mol%) was determined by the DSMZ by HPLC analysis using DNA isolated from CB1190T as described above.
Strain CB1190T grows slowly on AMS medium containing 1,4-dioxane. It also grows slowly on rich media such as LB, TSA and R2A in the absence of 1,4-dioxane. When grown in liquid medium, the cells appear as powdery white colonies floating on the liquid surface and form biofilms on the insides and the bottom of the flask. The cells produce white aerial mycelium and yellowish substrate mycelium, which branch and fragment into rod-shaped, non-motile units. No diffusible pigments or sporangia are produced. Hyphal swelling and budding are sometimes observed with this culture. The cells are 1–3 µm in size (a scanning electron micrograph is available as supplementary material in IJSEM Online).
CB1190T is an aerobic micro-organism capable of utilizing 1,4-dioxane as its sole source of carbon and energy for growth. In batch experiments, cell yield was 0·09±0·002 g protein (g dioxane)–1. The observed maximum growth rate was 90 µg l–1 h–1 and the maximum dioxane degradation rate was 0·1 µg dioxane (µg protein)–1 h–1, and is described by Monod kinetics. The addition of 10 mg vitamins stock l–1 (Tanner, 1997) to the AMS medium did not significantly affect the growth rate. CB1190T was capable of growing aerobically on benzene, toluene, formate, Casamino acids, LB broth and trypticase soy broth. No growth was observed on methyl tert-butyl ether or tert-butyl alcohol. While P. sulfidoxydans was able to use THF as a sole growth substrate but not 1,4-dioxane, P. hydrocarbonoxydans was unable to grow on either compound. The substrates in Biolog GP2 and SFP2 microplates metabolized by CB1190T, P. hydrocarbonoxydans and P. sulfidoxydans are listed in Table 1.
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and N2. The capability of CB1190T to fix atmospheric nitrogen was indicated by (i) slow but positive growth in ammonium-free AMS medium, as well as in the negative control well of the Biolog PM3 plate, (ii) production of ammonium ions in cell cultures grown in ammonium-free AMS medium and (iii) the presence of nitrogenase activity as measured by stoichiometric reduction of acetylene to ethene. The measured rate of ethylene production was 18 nmol h–1 (mg protein)–1. Abiotic loss of acetylene was negligible. No cell growth or ammonia production was observed in control vials containing N-free medium with headspace containing argon and 5 % oxygen. Neither P. hydrocarbonoxydans nor P. sulfidoxydans was able to grow in nitrogen-free medium in the presence of glucose or lactate as carbon source. Neither strain was capable of using N2 as a nitrogen source in the Biolog PM3 microplate test. Both strains were unable to reduce acetylene to ethylene, indicating the absence of nitrogenase activity. No other Pseudonocardia species has been reported to fix dinitrogen.
Growth on 1,4-dioxane in AMS was tested at temperatures ranging from 10 to 45 °C, and the optimum growth temperature was found to be 30 °C, with no observed growth at temperatures higher than 37 °C. CB1190T grown on 1,4-dioxane was able to oxidize naphthalene to a mixture of 1-naphthol and 2-naphthol, indicating soluble monooxygenase activity. A comparison of physiological properties of CB1190T with P. hydrocarbonoxydans and P. sulfidoxydans is presented in Table 1
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The whole-cell fatty acid pattern of CB1190T was of the iso-/anteiso-branched type. The dominant fatty acid was hexadecanoate (details available as supplementary material in IJSEM Online). Saturated, unsaturated and 10-methyl-branched fatty acids were also present. These signatures are diagnostic for members of the family Pseudonocardiaceae (Embley et al., 1988; Kroppenstedt, 1992). Ninety-nine per cent of the total peaks were named. The major PLFAs are hexadecanoate (27·5 %), 10-methylhexadecanoate (9·3 %) and 10-methylheptadecanoate (23·6 %). Methyl branching on the tenth carbon atom in a fatty acid molecule is specific for many mycolateless nocardioform actinomycetes. Like all other Pseudonocardia species, CB1190T does not synthesize mycolic acids. The dominant menaquinone was MK-8(H4). In addition, a small amount of MK-7(H4) was also present. The cell-wall peptidoglycan of strain CB1190T contained meso-diaminopimelic acid (m-Dpm). This indicates A1 peptidoglycan type, which is commonly found in representatives of Pseudonocardia.
The almost complete sequence of the 16S rRNA gene (1422 bp) was used for phylogenetic analyses. Preliminary phylogenetic placements based on the results of BLAST analyses revealed that strain CB1190T is closely related to the members of the family Pseudonocardiaceae. The closest phylogenetic neighbours with validly published names are P. sulfidoxydans (1401/1423 bp) and P. hydrocarbonoxydans (1400/1423 bp). Rigorous analysis of the phylogenetic position was carried out by constructing phylogenetic trees using 23 species containing 1353 nucleotides (Fig. 1). Kimura two-parameter neighbour-joining (Saitou & Nei, 1987) and maximum-likelihood (Felsenstein, 1981) methods were employed. Both methods consistently placed CB1190T in the cluster encompassing members of Pseudonocardia with high bootstrap support. This phylogenetic placement was not affected by the choice of different outgroups. The bootstrap confidence for the clade containing CB1190T, P. sulfidoxydans and P. hydrocarbonoxydans was 100 %.
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) and 98·4 % sequence similarity to its closest neighbours, P. sulfidoxydans (Reichert et al., 1998) and P. hydrocarbonoxydans (Lechevalier et al., 1986; Warwick et al., 1994). Moreover, strain CB1190T is unique among Pseudonocardia species in its ability to metabolize 1,4-dioxane and to fix dinitrogen. It is proposed that the organism be classified as Pseudonocardia dioxanivorans sp. nov.
Note added in proof
Since this article was submitted for publication, a novel species, Pseudonocardia benzenivorans, has been described (Kämpfer & Kroppenstedt, 2004).
Description of Pseudonocardia dioxanivorans sp. nov.
Pseudonocardia dioxanivorans (di.ox.a.ni.vo'rans. N.L. n. dioxanum 1,4-dioxane; L. part. adj. vorans devouring; N.L. part. adj. dioxanivorans dioxane-devouring).
The species description is based on the results of this study and Parales et al. (1994). Gram-positive, strictly aerobic, mycolateless actinomycete. Both aerial and vegetative mycelium fragment into rod-shaped elements. Capable of growing on 1,4-dioxane, THF, tetrahydropyran, 1,3-dioxane, 2-methyl-1,3-dioxolane, diethyl ether and butyl methyl ether. A variety of other organic compounds, such as ethers, alcohols, carbohydrates, carboxylic acids and amino acids, are also utilized (Table 1). Aerobic autotrophic growth occurs on H2 and CO2. This organism is able to fix dinitrogen. Acid is produced from (+)-D-glucose, (–)-L-rhamnose, (+)-D-xylose, (–)-D-fructose, (–)-D-trehalose, cellobiose, (–)-D-mannitol, maltose and salicin. Xanthine and hypoxanthine are decomposed. (–)-L-Tyrosine and adenine are not degraded. Optimal growth temperature is 30 °C. Nitrogenase-positive and oxygenase-positive. Predominant fatty acids are 16 : 0 iso, 16 : 1 iso cis9 and 17 : 1 iso cis9. The major menaquinone [MK-8(H4)] has eight isoprene units, two of which are hydrogenated. Cell wall contains meso-Dpm. The G+C content is 74 mol%.
The type strain, CB1190T (=ATCC 55486T=DSM 44775T), was isolated from a 1,4-dioxane-contaminated sludge sample collected at Darlington, SC, USA (Parales et al., 1994).
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ACKNOWLEDGEMENTS |
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-D-mannosamine, L-arabinose, D-arabitol, D-galacturonic acid, methyl 