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-proteobacterium
1 Mikrobiologie, Institut für Biologie II, Universität Freiburg, Schänzlestr. 1, D-79104 Freiburg, Germany
2 DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany
Correspondence
Georg Fuchs
georg.fuchs{at}biologie.uni-freiburg.de
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ABSTRACT |
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-subclass of Proteobacteria. Based on the high 16S rDNA sequence divergence and phenotypic characteristics, the name Alicycliphilus denitrificans gen. nov., sp. nov. is proposed for this strain. The type strain is K601T (=DSM 14773T =CIP 107495T).
The EMBL accession number for the 16S rDNA sequence of strain K601T is AJ18042.
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The aerobic degradation of alicyclic compounds has been extensively studied in several aerobic bacterial genera such as Acinetobacter (Donoghue & Trudgill, 1975
), Pseudomonas (Tanaka et al., 1977) and Xanthobacter (Trower et al., 1985). The aerobic degradation of alicyclic compounds requires molecular oxygen and monooxygenases for the cleavage of the ring. Anaerobic degradation of alicyclic compounds has been less well studied and little information on this field is available (Evans, 1977; Trudgill, 1984; Dangel et al., 1988, 1989; Foss & Harder, 1998; Foss et al., 1998). Three isolates growing under denitrifying conditions with alicyclic compounds such as cyclohexanol have been obtained (Dangel et al., 1988) and two of them were studied (Dangel et al., 1988, 1989). Since the isolates were rather similar to each other, only one isolate, referred to as strain K601T, has been studied in greater detail. In this paper we report the description of this strain as Alicycliphilus denitrificans gen. nov., sp. nov.
Strain K601T, previously identified as a Pseudomonas species, was isolated from a waste water treatment plant with cyclohexanol as sole carbon source and nitrate as electron acceptor (Dangel et al., 1988). The medium used for enrichment, isolation and routine cultivation contained (l-1 distilled water): 1·08 g KH2PO4, 5·6 g K2HPO4, 0·54 g NH4Cl, 0·15 g CaCl2.2H2O, 0·2 g MgSO4.7H2O, 1·27 g NaNO3, 1 ml trace element solution SL-10 (Widdel et al., 1983), 1 ml selenite/tungstate solution (Tschech & Pfennig, 1984), 1 ml vitamin solution VL-7 (Pfennig, 1978) and carbon source (1 mM cyclohexanol). The final pH was 7·2–7·4. The medium was made anaerobic by applying several cycles of vacuum and flushing with oxygen-free nitrogen gas at room temperature. For aerobic growth, the same medium composition was used except that it did not contain NaNO3. Cultures were routinely grown at 30 °C and aerobically grown cultures were shaken at 120 r.p.m. To determine the substrate spectrum of strain K601T the following compounds (concentrations in mM in parentheses) were tested under aerobic and anoxic conditions in the mineral medium described above: cyclohexanol (1), cyclohexanone (1), 1,3-cyclohexanedione (1), 2-cyclohexenone (1), 1,3-cyclohexanediol (cis and trans) (1), 1,2-cyclohexanediol (1), 1,2-cyclohexanedione (1), 2-hydroxycyclohexanone (1), 1,4-cyclohexanedione (1), cyclohexane (1), monocarboxylic acids (C2–C7) (2), adipate (2), pimelate (2), 5-oxocaproate (2), citrate (2), 2-oxoglutarate (2), succinate (2), malate (2), crotonate (2), lactate (2), pyruvate (2), fumarate (2), phenol (1), aniline (1), malate (2), propionate (2), benzoate (1), 2-aminobenzoate (1), 2-hydroxybenzoate (1), 3-hydroxybenzoate (1), 4-hydroxybenzoate (1), resorcinol (1), hydroxyquinol (1), m-cresol (1), o-cresol (1), p-cresol (1), vanillate (1), indole (1), 4-aminobenzoate (1), resorcinol (1), 2-naphthoic acid (1), biphenyl 2-carboxylic acid (1), gentisate (1), protocatechuate (1), 3-fluorobenzoate (1), 3-chlorobenzoate (1), formate (2), glucose (2), fructose (2), xylose (2) and aliphatic alcohols (C1–C8) (2). The electron acceptors tested were nitrate, nitrite, sulfate, sulfite, fumarate (all at 5 mM) and oxygen. All substrates were anaerobically prepared and were autoclaved or filter-sterilized.
For fatty acid analysis the strain was grown on R2A medium and cells were harvested after 3 days by centrifugation. About 40 mg (w/w) of the cells was saponified, methylated, extracted and analysed by using the Microbial Identification System (MIS) described by Miller (1982).
For determination of DNA base composition, the DNA was isolated and purified by chromatography on hydroxyapatite and the G+C content was determined by HPLC (Mesbah et al., 1989). Non-methylated 
DNA (Sigma) was used as standard. For DNA–DNA hybridization, DNA was isolated by the method of Cashion et al. (1977). DNA–DNA hybridization was carried out as described by De Ley et al. (1970), with the modifications described by Escara & Hutton (1980) and Huss et al. (1983) using a Gilford System model 2600 equipped with a Gilford model 2527-R thermoprogrammer and plotter. Reassociation was carried out in 2x times; SSC containing 10 % dimethylsulfoxide at 68 °C. Renaturation rates were computed with the TRANSFER.BAS program (Jahnke & Bahnweg, 1986; Jahnke, 1992).
Phase-contrast microscopy was performed by using a Zeiss microscope equipped with a camera. Wet mounts for photomicrographs of the micro-organisms were made according to Pfennig & Wagener (1986).
Growth was measured spectrophotometrically at 580 nm using cuvettes with a 1 cm light path. Aromatic compounds were measured using an HPLC system equipped with a UV detector set at 280 nm. Separation was achieved using a Beckman Ultrasphere column (4·6x250 mm, 5 µm particle size) maintained at room temperature. The mobile phase, consisting of a mixture of two solvents (water and 0·01 %, v/v, acetic acid in 50 %, v/v, acetonitrile) was used at a flow rate of 1 ml min-1. For separation of aromatic compounds, 25 % acetonitrile solvent phase was initially held for 20 min, then the concentration was increased to 50 % over a period of 5 min and held for 5 min. The column was re-equilibrated with 25 % methanol for at least 5 min before the next injection. Nitrate and nitrite were estimated using the Quantofix test (Macherey–Nagel).
Genomic DNA extraction, PCR-mediated amplification of the 16S rDNA and sequencing of PCR products were carried out as described by Rainey et al. (1996). Purified PCR products were sequenced directly using the Taq DyeDeoxy Terminator Cycle Sequencing Kit (Applied Biosystems), according to the manufacturer's instructions. The Applied Biosystems 310 DNA Genetic Analyser was used for the electrophoresis of the sequence reaction products. The almost complete 16S rDNA sequences of the isolates were aligned manually with those of all currently available nucleotide sequences of representatives of the -Proteobacteria retrieved from GenBank and EMBL databases using the ae2 editor (Maidak et al., 1999). The method of Jukes & Cantor (1969) was used to calculate evolutionary distances on the basis of 1298 nt. Phylogenetic dendrograms were reconstructed according to the method of DeSoete (1983) and the neighbour-joining and maximum-likelihood methods contained in the PHYLIP package (Felsenstein, 1993). Following determination of the phylogenetic position within the -Proteobacteria the dendrogram was restricted to the nearest neighbours. The accession numbers of these reference organisms are indicated in Fig. 1.
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). The inoculum used for the enrichment was from a municipal sewage plant in Konstanz (Germany). The medium used was as described by Tschech & Fuchs (1987). The growth conditions were 28–30 °C and pH 7·2–7·4. Cells of strain K601T were short rods, 0·6 µm wide and 1–2 µm long, motile and stained Gram-negative. Catalase and oxidase reactions were positive. Strain K601T was a facultative anaerobe. The metabolism was strictly oxidative. Nitrate, nitrite and oxygen were used as electron acceptors while sulfate, sulfite and fumarate were not reduced. Strain K601T was capable of aerobic and anaerobic growth on a large range of organic substrates. Physiological reactions observed under anoxic denitrifying conditions and under aerobic conditions are indicated in the species description. The G+C content of strain K601T was 66 mol% as determined by HPLC.
The major fatty acids were hexadecenoic acid (C16 : 1
7c; 37 %); hexadecanoic acid (C16 : 0, 24 %) and octadecenoic acid (C18 : 17c, 21 %). The structure of the latter fatty acid is identical to cis-vaccenic acid (
11-C18 : 1), reported by Willems et al. (1989). 3-Hydroxydecanoic acid (3-OH C10 : 0) and saturated acids (C12 : 0; 4 %; C15 : 0, 2 %; and cycloC17 : 0, 2 %) occurred in smaller amounts. The presence of the three major components have also been reported for members of Comamonas and Delftia (Tamaoka et al., 1987), as well as for Hydrogenophaga (Willems et al., 1989).
16S rDNA sequence analysis showed that strain K601T clusters within the family Comamonadaceae in the -subclass of the Proteobacteria (Willems et al., 1991). This family comprises the genera Acidovorax, Comamonas, Delftia, Hydrogenophaga, Rhodoferax, Brachymonas, Polaromonas, Variovorax, Xylophilus (Wen et al., 1999), Xenophilus (Blümel et al., 2001) and misclassified members of Aquaspirillum. Strain K601T represents an individual line of descent, showing less than 96 % sequence similarity to any other member of this family. Phylogenetically it branches between [Aquaspirillum] psychrophilum LMG 5408T and a cluster consisting of Comamonas, Brachymonas, Hydrogenophaga, Delftia and Xenophilus. The statistical significance of most branching points is low (<75 %), hence the branching pattern should not be considered stable and some of the lineages may change position as new sequences are included. The low 16S rDNA similarities found between strain K601T and other members of the family Comamonadaceae exclude a high degree of DNA–DNA reassociation similarity that would affiliate this strain to any described species of the various genera within this family (Stackebrandt & Goebel, 1994). This notion is confirmed by the low degree of DNA relatedness of 26 %, determined for strain K601T and Delftia acidovorans DSM 50251T which emerges as the phylogenetic neighbour (Fig. 1
).
Analysis of the 16S rRNA gene sequences showed that strain K601T is a member of the family Comamonadaceae in the -subclass of the Proteobacteria. The reason for creating a new genus for strain K601T was the high sequence divergence from related genera (more than 4 % sequence divergence). A pattern of phenotypic differences between strain K601T was also noticed (Table 1), such as differences in carbon source utilization, the ability to denitrify and base composition of DNA. Though members of this family are phylogenetically closely related, they are phenotypically heterogeneous. Their presence in different habitats seems to contribute to the natural biodegradation process of many natural compounds and pollutants since Comamonadaceae have been isolated from different environments (soil, wastewater, activated sludge, oil brine, crude oil) and on a wide variety of substrates, including carboxylic or dicarboxylic acids, aliphatic or unsaturated acids, sterols and monoaromatic compounds, as well as aromatic polymers of the lignin type (Willems et al., 1992).
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Cells are short rods (0·6x1–2 µm), motile, Gram-negative, catalase- and oxidase-positive. Optimal growth occurs at 28–30 °C and pH 7·2–7·4 under aerobic or anoxic conditions. Metabolism is strictly oxidative. Electron acceptors nitrate, nitrite and oxygen are used; sulfate, sulfite and fumarate are not reduced. G+C content is near 66 mol%. Phylogenetically related to the family Comamonadaceae. Type species is Alicycliphilus denitrificans.
Description of Alicycliphilus denitrificans sp. nov.
Alicycliphilus denitrificans (de.ni.tri'fi.cans.L.prep.de away from; L.n.nitrum soda; N.L.n.nitrum nitrate; N.L.v. denitrifico to denitrify; N.L. part. adj. denitrificans denitrifying).
The description is the same as given above for the genus. The following substrates are used under anoxic conditions: cyclohexanol, cyclohexanone, 1,3-cyclohexanedione, 2-cyclohexenone, 1,3-cyclohexanediol (cis and trans), monocarboxylic acids (C2–C7), adipate, pimelate, 5-oxocaproate, citrate, 2-oxoglutarate, succinate, L-malate, propionate, crotonate, L-lactate, pyruvate and fumarate. The following compounds are not used: aniline, phenol, benzoate, 2-aminobenzoate, 2-hydroxybenzoate, 3-hydroxybenzoate, 4-hydroxybenzoate, resorcinol, hydroxyquinol, m-cresol, o-cresol, p-cresol, vanillate, naphthoate, indole, 1,2-cyclohexanediol, 1,2-cyclohexanedione, 2-hydroxycyclohexanone, 1,4-cyclohexanedione, cyclohexane, formate, D-glucose, D-fructose, D-xylose and aliphatic alcohols (C1–C8). Under aerobic conditions the following compounds are used: propionate, L-malate, aniline, fumarate, indole, vanillic acid, acetate, 4-hydroxybenzoate, m-cresol, o-cresol, p-cresol, crotonate, D-glucose, L-lactate and pyruvate. The following compounds are not used: 4-aminobenzoate, benzoate, resorcinol, 2-naphthoate, biphenyl 2-carboxylate, 2-aminobenzoate, 3-hydroxybenzoate, gentisate, protocatechuate, hydroxyquinol, 3-fluorobenzoate and 3-chlorobenzoate. G+C content is 66 mol%. Isolated from an enrichment culture inoculated with a liquid sample from a municipal sewage plant in Konstanz (Germany). Type strain is K601T (=DSM 14773T =CIP 107495T)
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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