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1 Bereich Mikrobiologie, Helmholtz Zentrum für Infektionsforschung (formerly GBF), D-38124 Braunschweig, Germany
2 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität Wien, A-1210 Wien, Austria
3 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität, D-35390 Giessen, Germany
4 Department of Biological and Environmental Science, University of Jyväskylä, F-40500 Jyväskylä, Finland
5 Línea de Degradación de Tóxicos Orgánicos, Depto. de Protección Ambiental, Estación Experimental del Zaidín – EEZ, Consejo Superior de Investigaciones Científicas, Calle Profesor Albareda 1, E-18008 Granada, Spain
Correspondence
Wolf-Rainer Abraham
wab{at}gbf.de
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains A175T and K101T are X94101 and AJ009706, respectively.
An additional phylogenetic tree and tables detailing polar lipid distribution, FAB of phospholipids and polyamine patterns for the novel species are available with the online version of this paper.
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TOPABSTRACTMAIN TEXTREFERENCES |
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) and many of them were originally assigned to the genus Sphingomonas (Balkwill et al., 1997; Karlson et al., 1996; Moore et al., 1993; Nohynek et al., 1996a, b; Stolz et al., 2000; Zipper et al., 1996). However, with the exception of Sphingomonas wittichii, all of these isolates have since been reclassified as species of the genera Sphingobium or Novosphingobium (Pal et al., 2006; Takeuchi et al., 2001). There are some indications that the intermediary halocatechols, especially 4-fluorocatechol and 4-chlorocatechol, originating from the bacterial breakdown of some haloaromatics, can be mineralized through a proposed novel pathway involving protoanemonin (Blasco et al., 1995; Nikodem et al., 2003; Wittich et al., 1999). This mechanism is possible in several strains that express only the genes encoding the ortho-pathway for the breakdown of catechol. Inducing extradiolically-cleaving catechol dioxygenase activity would lead to the misrouting of halogenated intermediates in those strains lacking a functional chlorocatechol pathway. In sphingomonads, a chlorocatechol pathway (in sensu stricto) has been detected only in the 1,4-dichlorobenzene-mineralizing strain A175T and may also be found in some chlorophenoxy herbicide-degrading isolates (Ka et al., 1994) and in Gram-positive bacteria (Konig et al., 2004).
Strain A175T was isolated from a mixture of various soil and water samples that used 1,4-dichlorobenzene as the sole carbon and energy source (Schraa et al., 1986). The novel strain was initially identified as a member of the genus Alcaligenes and only later was it was discovered that the strain actually belongs to the family Sphingomonadaceae (Kosako et al., 2000). Strain K101T was isolated from 2,4,6-trichlorophenol-, 2,3,4,6-tetrachlorophenol- and pentachlorophenol-contaminated boreal groundwater in Finland and this novel strain was able to degrade all of these compounds (Männistö et al., 1999). Here, we report the results of a polyphasic study of these two novel isolates which are currently assigned to the genus Sphingomonas (Takeuchi et al., 2001; Yabuuchi et al., 1990).
Biomass for the extraction of quinones, polar lipids and polyamines was grown on PYE medium (Busse et al., 2005). For the extraction of fatty acids, biomass was grown on trypticase soy agar. Liquid and solid Luria–Bertani (LB) or R2A media were used for culturing the strains for the other taxonomic tests described in this study. Solid mineral salts medium plates were used to check the degradation of individual organic carbon sources at a concentration of organic carbon corresponding to about 25 mM single carbon atom. Cultures were grown aerobically at 28 °C. Cell morphology and dimensions were determined by phase-contrast microscopy. Cells were rod-shaped, 0.8–1.5 µm in length and 0.4–0.6 µm in diameter. Cells of both strains showed a tendency to grow in rosette-like formations. However, when grown on selective media, cells of both novel strains tended to grow as branched thread-like/hyphae-like aggregates.
The procedures used for physiological and biochemical characterizations were those described earlier (Kämpfer & Altwegg, 1992; Kämpfer et al., 1991). The results obtained using API galleries (bioMérieux) and Biolog substrate utilization tests are given in detail in the species description. Strain A175T has been reported to grow on 1,4-dichlorobenzene, but not on chlorophenols (Schraa et al., 1986), and strain K101T has been found to use tri-, tetra- and pentaphenols (Männistö et al., 1999).
Interestingly, strain K101T was capable of assimilating only two of the long list of carbon sources tested, namely acetate and DL-3-hydroxybutyrate, and is thus unique in the genus Sphingomonas (Denner et al., 1999; Kämpfer et al., 1997) (Table 1). With this highly specialized characteristic, strain K101T resembles strains of another sphingomonad species, Novosphingobium lentum, which was isolated from a chlorophenol-degrading bioreactor purifying water from the same aquifer (Tiirola et al., 2005).
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. The purity of the DNA samples was confirmed with caesium chloride gradient centrifugation. DNA G+C content was determined as described by Johnson (1994) using 
phage DNA as a standard. The separation was performed on a Purospher endcapped reverse-phase HPLC column (Merck) of 250x4 mm. The mobile phase was 20 mM triethylamine phosphate in 12 % aqueous methanol at a flow rate of 1 ml min–1 at 22 °C. The DNA G+C contents were 66.1 mol% for strain A175T and 63.6 mol% for strain K101T. These values are within the range commonly found for members of the family Sphingomonadaceae but did not allow a clear affiliation to be made to a specific genus.
For the amplification of the 16S rRNA gene by PCR, single colonies were boiled in 100 µl of TE buffer for about 10 min at 95 °C to obtain DNA. A nearly complete 16S rRNA gene sequence was obtained as described previously (Abraham et al., 1999). Reactions were evaluated on an Applied Biosystems 377 Genetic Analyzer and the final contig was assembled using the SEQUENCHER program version 4.0.5 (Gene Codes Corporation). The sequences were matched against the EMBL database (Kanz et al., 2005) using BLAST 2.2.9 (Altschul et al., 1990). The 16S rRNA gene sequences of strains A175T and K101T have already been deposited in the EMBL database under the accession numbers X94101 (Nohynek et al., 1996a) and AJ009706 (Männistö et al., 1999), respectively. The sequences were aligned using CLUSTAL_X software (Thompson et al., 1997). Tree topologies were reconstructed with the neighbour-joining algorithm with 1000 bootstrap replications, according to the method of Junca and Pieper (2004) (Fig. 1) and the UPMGA algorithm with the Kimura two-parameter model was calculated using MEGA 3.1 software (Kumar et al., 2004) (see Supplementary Fig. S1 in IJSEM Online) using the EMBL database (Kanz et al., 2005). The 16S rRNA gene sequence of strain A175T showed 93.3 % similarity to that of Sphingomonas paucimobilis GIFU 2395T, 96.0 % to strain K101T and 96.7 % to the closest recognized species, S. wittichii RW1T (Yabuuchi et al., 2001). These relatively low gene sequence similarities indicate that strain A175T represents a novel species. Strain K101T showed a 16S rRNA gene sequence similarity of 93.1 % to S. paucimobilis GIFU 2395T and 95.8 % to S. wittichii RW1T.
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. Strains A175T (Busse et al., 1999) and K101T represent species containing sym-homospermidine as the major polyamine and they share this characteristic with the other species of the genus Sphingomonas sensu stricto (Busse et al., 1999; Takeuchi et al., 2001) and the genus Sphingosinicella (Geueke et al., 2007). Strain A175T appeared to be unique in the entire genus with respect to its unusually high content of cadaverine (see Supplementary Table S2 in IJSEM Online). Respiratory quinones were extracted as reported by Ventosa et al. (1993) and Altenburger et al. (1996). While strain A175T formed only ubiquinone Q-10, strain K101T also contained small amounts of Q-9 (2 %).
GC was used to analyse the fatty acid profiles of the novel strains, as described previously (Kämpfer et al., 1992). The fatty acid C16 : 1
9c was shared by S. wittichii RW1T and strain K101T only. These two strains also contained fatty acid C16 : 111c, which has not been found previously within members of the genus Sphingomonas (Busse et al., 1999). Fatty acid C18 : 0 was found in S. wittichii RW1T, strain A175T and strain K101T. In contrast to strain A175T, strain K101T did not contain fatty acids C16 : 15c, C17 : 16c, C17 : 18c, C18 : 15c or those fatty acids that comprise summed feature 4 (Table 2).
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and analysed by two-dimensional TLC. Unique polar lipid profiles distinguished strains A175T and K101T from each other and from S. wittichii RW1T. Lack of phosphatidylmonomethylethanolamine and phosphatidyldimethylethanolamine in extracts from strain A175T enabled this strain to be differentiated from S. wittichii RW1T (Busse et al., 1999) and strain K101T. The absence of detectable amounts of phosphatidylcholine and the unknown lipids PL3, GL1 and GL4 in extracts from strain K101T was unique among these closely related strains (see Supplementary Table S1a in IJSEM Online).
Lipids were extracted by a modified Bligh–Dyer method (Fredrickson et al., 1986), followed by analysis in a mass spectrometer using fast atom bombardment (FAB-MS) ionization recorded in the negative mode of selected fractions as previously described by Abraham et al. (1997). Analysis of the individual phospholipids by MS revealed that C18 : 1–C16 : 1-phosphatidyl-N,N-dimethylethylamine (743 Da), the corresponding choline (756 Da), C18 : 1–C18 : 1-phosphatidic acid (700 Da), the corresponding -N,N-dimethylethylamine (771 Da) and corresponding choline (785 Da) were formed by nearly all members of the family Sphingomonadaceae investigated. Interestingly, for the separated group of strains in the Sphingomonas cluster, S. wittichii RW1T and strains K101T and A175T, some lipids could be identified as occurring preferentially in these strains. These were C19 : 1–C16 : 0-phosphatidic acid (688 Da) and -glycerol (762 Da), C18 : 1–C16 : 1-N-methylethylamine (729 Da) and C18 : 1–C16 : 2-phosphatidyl-N,N-dimethylethylamine (741 Da) (see Supplementary Table S1b in IJSEM Online).
On the basis of the 16S rRNA gene sequences, strains A175T and K101T were found to be only remotely related to other species of the genus Sphingomonas. Although strain A175T is more closely related to S. wittichii RW1T than to strain K101T on the basis of 16S rRNA gene sequence comparisons, strain A175T differs significantly from these sphingomonads in its polyamine pattern (see Supplementary Table S2 in IJSEM Online).
Our data do not support the notion of Takeuchi et al. (2001) that members of the genus Sphingomonas and those of the genera Sphingobium, Novosphingobium and Sphingopyxis can be discerned by the presence of sym-homospermidine and the absence of spermidine in Sphingomonas species while species of the other three genera possess spermidine but not homospermidine (see Supplementary Table S2). Both polyamines were detected in S. wittichii RW1T and in strains A175T and K101T, but were also detected in the type strains of Sphingomonas asaccharolytica, Sphingomonas paucimobilis, Sphingomonas trueperi, Sphingomonas abaci, Sphingomonas panni, Sphingomonas echinoides and Sphingomonas pituitosa (Busse et al., 1999, 2005; Denner et al., 1999, 2001). However, all species of the genus Sphingomonas sensu stricto are characterized by the predominant polyamine sym-homospermidine. These results show that species of the genus Sphingomonas have mainly sym-homospermidine and some of them also produce minor quantities of spermidine. Species of the genera Sphingobium, Novosphingobium and Sphingopyxis produce no sym-homospermidine. However, sym-homospermidine also characterizes species of the genus Sphingosinicella (Geueke et al., 2007; Maruyama et al., 2006). Although strains K101T and A175T share most of the signature nucleotides proposed by Takeuchi et al. (2001) for the differentiation of members of the genus Sphingomonas sensu stricto from related genera, these nucleotides are also found in species of the genus Sphingosinicella (Geueke et al., 2007; Maruyama et al., 2006). In conclusion, neither the polyamine patterns nor the signature nucleotides allow the assignment of strains K101T and A175T to either of the two genera. The phylogenetic distance of the two novel strains to representatives of the genus Sphingosinicella and their close relatedness to S. wittichii, as well as differences in the signatures identified for members of the genus Sphingosinicella by Geueke et al. (2007) support the assignment of strains K101T and A175T to the genus Sphingomonas. Therefore, the names Sphingomonas fennica sp. nov. and Sphingomonas haloaromaticamans sp. nov. are proposed for strains K101T and A175T, respectively.
Description of Sphingomonas haloaromaticamans sp. nov.
Sphingomonas haloaromaticamans (ha.lo.aro.ma.tic.a'mans. N.L. n. haloaromaticum haloaromatic, class of chemical compound; L. part. adj. amans loving; N.L. part. adj. haloaromaticamans loving haloaromatics).
Cells are rod-shaped, 0.8–1.5 µm in length and 0.4–0.6 µm in diameter. Colonies are yellow-coloured. N-Acetyl-D-glucosamine, L-arabinose, p-arbutin, D-cellobiose, D-galactose, D-glucose, D-maltose, 
-D-melibiose, D-xylose, acetate, propionate, azelate, DL-3-hydroxybutyrate, DL-lactate, pyruvate, L-alanine, L-aspartate, L-histidine, L-leucine, L-proline and L-tryptophan are used as substrates, but not D-fructose, gluconate, D-mannose, L-rhamnose, sucrose, salicin, D-trehalose, maltitol, D-mannitol, D-sorbitol, cis-aconitate, adipate, 4-aminobutyrate, citrate, fumarate, L-malate, L-ornithine, L-phenylalanine, 3-hydroxybenzoate, 4-hydroxybenzoate or phenylacetate. Aesculin, pNP--D-glucopyranoside, pNP-
-D-glucopyranoside, bis-pNP-phosphate, pNP-phenylphosphonate, 2-deoxythymidine-5'-pNP-phosphate, L-alanine-pNA, L-glutamate-
-3-carboxy-pNA and L-proline-pNA are hydrolysed, but pNP--D-galactopyranoside, pNP--D-glucuronide and pNP-phosphorylcholine are not hydrolysed. Nitrate is not reduced. The main polar lipids are phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol and sphingoglycolipid. Phosphatidylcholine, unidentified phospholipid PL3 and unidentified glycolipid GL4 are minor constituents. Major fatty acids are C18 : 1 (summed feature 7) and C16 : 1 (summed feature 4). Minor fatty acids are C14 : 0, C15 : 0, C16 : 0, C18 : 0, C16 : 15c, C17 : 16c, C17 : 18c and C18 : 15c. The major hydroxy-fatty acid is C14 : 0 2-OH together with minor amounts of C15 : 0 2-OH. The major polyamine is homospermidine; minor polyamines are diaminopropane, putrescine, cadaverine, spermidine and spermine. Produces only ubiquinone Q-10. The DNA G+C content of the type strain is 66.1 mol%. Grows between 10 and 40 °C with optimal growth between 30 and 37 °C. The optimal pH range is 5–8.
The type strain, A175T (=DSM 13477T=CCUG 53463T), was isolated from water and soil samples from the Netherlands as a degrader of benzene, catechol, chlorobenzene, 1,3-dichlorobenzene and 1,4-dichlorobenzene.
Description of Sphingomonas fennica sp. nov.
Sphingomonas fennica (fen.ni'ca. N.L. fem. adj. fennica pertaining to Finland, from where the type strain was isolated).
Colonies are coloured light yellow but the colour is not stable during subcultivation on rich medium. Short, plump, rod-shaped cells, 0.5–0.9 µm by 0.9–1.5 µm. Cells are motile. Reduces nitrate to nitrogen. Acetate and DL-3-hydroxybutyrate are used as substrate but not N-acetyl-D-glucosamine, L-arabinose, p-arbutin, D-cellobiose, D-fructose, D-galactose, gluconate, D-glucose, D-mannose, D-maltose, -D-melibiose, L-rhamnose, sucrose, salicin, D-trehalose, D-xylose, maltitol, D-mannitol, D-sorbitol, propionate, cis-aconitate, adipate, 4-aminobutyrate, azelate, citrate, fumarate, DL-lactate, L-malate, pyruvate, L-alanine, L-aspartate, L-histidine, L-leucine, L-ornithine, L-phenylalanine, L-proline, L-tryptophan, 3-hydroxybenzoate, 4-hydroxybenzoate or phenylacetate. pNP-phosphorylcholine, 2-deoxythymidine-5'-pNP-phosphate and L-alanine-pNA are hydrolysed, but aesculin, pNP--D-galactopyranoside, pNP--D-glucuronide, pNP--D-glucopyranoside, pNP--D-glucopyranoside, bis-pNP-phosphate, pNP-phenylphosphonate, L-glutamate--3-carboxy-pNA and L-proline-pNA are not hydrolysed. Polar lipids are phosphatidylmonomethylethanolamine, phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, phosphatidyldimethylethanolamine and sphingoglycolipid. Major fatty acids are C18 : 1 (summed feature 7), C16 : 19c and C16 : 0. Minor fatty acids are C14 : 0, C18 : 0, and C16 : 111c. The major hydroxy-fatty acid is C14 : 0 2-OH, with minor amounts of 2-C15 : 0 2-OH and C16 : 0 2-OH. Major polyamine is homospermidine; minor polyamines are putrescine, cadaverine, spermidine and spermine. Produces ubiquinone Q-10, but small amounts (2 %) of Q-9 can also be detected. DNA G+C content of the type strain is 63.6 mol%. Grows between 10 and 37 °C with optimal growth between 20 and 30 °C. pH range for growth is 5–8, optimal pH is 7–8.
The type strain, K101T (=DSM 13665T=CCUG 53462T), was isolated from polychlorophenol-contaminated groundwater adjacent to a sawmill, Southern Finland, as a degrader of 2,4,6-trichlorophenol, 2,3,4,6-tetrachlorophenol and pentachlorophenol. The environment from which the strain was originally isolated was cold (7–8 °C), oxygen-deficient, humic (4–23 mg dissolved organic carbon l–1) and slightly acidic (pH 6–6.5).
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ACKNOWLEDGEMENTS |
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