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1 Department of Biological and Environmental Science, University of Jyväskylä, FIN-40014 Jyväskylä, Finland
2 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, A-1210 Vienna, Austria
3 Institut für Mikrobiologie und Genetik, Universität Wien, A-1030 Vienna, Austria
4 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität Giessen, D-35392 Giessen, Germany
5 Finnish Forest Research Institute, Eteläranta 55, FIN-96300 Rovaniemi, Finland
Correspondence
Marja Tiirola
mtiirola{at}jyu.fi
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-4 subclass of the Proteobacteria and were members of the genus Novosphingobium. The highest 16S rRNA gene sequence similarity observed for these strains was 96·5 % with the type strains of Novosphingobium hassiacum, Novosphingobium aromaticivorans and Novosphingobium subterraneum. Chemotaxonomic data (major ubiquinone: Q-10; major polyamine: spermidine; major polar lipids: phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, phosphatidylcholine and sphingoglycolipid; major fatty acids: 18 : 1
7c, 16 : 17c and 2-OH 14 : 0) as well as the ability to reduce nitrate supported the affiliation of the strains to the genus Novosphingobium. Based on the phylogenetic analysis, whole-cell fatty acid composition as well as biochemical and physiological characteristics, the MT1-like strains were highly similar and could be separated from all recognized Novosphingobium species. The novel species Novosphingobium lentum sp. nov. is proposed to accommodate strains MT1T (=DSM 13663T=CCUG 45847T), MT101 (=CCUG 45849), MT103 (=CCUG 45850) and MT104 (=CCUG 45851).
Published online ahead of print on 8 October 2004 as DOI 10.1099/ijs.0.63386-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain MT1T is AJ303009.
Phylogenetic trees, a Euclidean distance dendrogram, a polar lipid profile and whole-cell fatty acid profiles of the strains studied are available as supplementary material in IJSEM Online.
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to accommodate strictly aerobic, chemoheterotrophic, yellow-pigmented, Gram-negative, rod-shaped bacteria that contain glycosphingolipids as cell envelope components, but the classification did not consider their heterogeneity in polyamine patterns (Busse & Auling, 1988). On the grounds of 16S rRNA gene sequences, the genus could be separated into at least four clusters (Takeuchi et al., 1994; Yurkov et al., 1997). Based on phylogenetic, chemotaxonomic and physiological analyses, the genus Sphingomonas has been divided into four genera: Sphingomonas, Sphingobium, Novosphingobium and Sphingopyxis (Takeuchi et al., 2001). Yabuuchi et al. (2002) suggested that the genus Sphingomonas should remain undivided and that the other three proposed genera, Sphingobium, Novosphingobium and Sphingopyxis, should be considered as later homotypic synonyms of species of the genus Sphingomonas because of the lack of sufficient evidence of the phenotypic features separating these groups. In this paper, however, we adhere to the taxonomic interpretation of Takeuchi et al. (2001), because the four major groups within the Sphingomonadaceae are phylogenetically clearly separated and the proposal of Yabuuchi et al. (2002) ignores that the genus Sphingomonas sensu Takeuchi et al. (2001) is clearly separated from the other three genera by the presence of sym-homospermidine instead of spermidine, characteristic for species of the genera Sphingobium, Novosphingobium and Sphingopyxis (Busse et al., 1999; Takeuchi et al., 2001). At the time of writing, the genus Novosphingobium comprises nine species, Novosphingobium aromaticivorans (Balkwill et al., 1997), Novosphingobium capsulatum (Leifson, 1962; Yabuuchi et al., 1990), Novosphingobium hassiacum (Kämpfer et al., 2002), Novosphingobium rosa (Takeuchi et al., 1995), Novosphingobium stygium (Balkwill et al., 1997), Novosphingobium subarcticum (Nohynek et al., 1996), Novosphingobium subterraneum (Balkwill et al., 1997), Novosphingobium tardaugens (Fujii et al., 2003) and Novosphingobium pentaromaticivorans (Sohn et al., 2004). Most of these species have been isolated from aquatic environments and many have been of special interest because of their potential to degrade toxic compounds.
Recently, we have studied a fluidized-bed bioremediation process treating polychlorophenol-contaminated groundwater at ambient groundwater temperature (4–8 °C) in Kärkölä, Finland, and isolated a dominant bacterial strain, designated MT1T, from the process (Tiirola et al., 2002). The strain degraded 2,4,6-trichlorophenol, 2,3,4,6-tetrachlorophenol and pentachlorophenol, which were the primary carbon and energy sources in the process water (Tiirola et al., 2002). One year later, three additional MT1-like strains, MT101, MT103 and MT014, were isolated from the same bioreactor. During characterization of the strains, they were cultivated in R2A broth or on R2A agar (Reasoner & Geldreich, 1985) at 22 °C. The strains formed pale-yellow colonies within 6–7 days on R2A at 22 °C, and their doubling time in R2A broth at 22 °C (125 r.p.m.) varied between 6·7 and 7·4 h (Tiirola et al., 2002). Colonies were either slimy, flat and smooth, or dry and elevated. Cultivation of the slimy colonies in liquid medium yielded homogeneous cultures in which cells grew singly or in pairs (planktonic form). Cultivation of the dry colonies yielded rosette formations and large rafts of thousands of cells (sessile form). The optimum growth temperature for strain MT1T was 23 °C; growth was observed at 4–30 °C but not at 33 °C (Männistö & Puhakka, 2002). Growth was not detected in tryptone soy agar (TSA) or half-strength TSA. Motility was determined using the hanging drop technique (Frerichs, 1984). For transmission electron microscopy, negative staining was performed by applying a drop of the culture in exponential growth phase onto a carbon-coated copper grid and staining with 1 % (w/v) phosphotungstic acid adjusted to pH 6·5 with potassium hydroxide.
Physiological and biochemical characterization was performed on the basis of 66 biochemical and physiological characteristics, as described by Kämpfer et al. (1997). Other biochemical properties were examined using the API 20NE system (bioMérieux) at 22 °C using incubation periods of 2 and 4 days. Physiological characteristics of strain MT1T and the type strains of other Novosphingobium species are summarized in Table 1. Strains MT101, MT103 and MT104 were also tested and they gave identical reactions to MT1T. Oxidase reaction was tested with API #7046 Kovac's reagent, Pyo-Test MW990 strips (Medical Wire & Equipment Co.) and Bactident-Oxidase strips (Merck). Negative results were obtained with the oxidase test with Kovac's reagent and Pyo-Test strips, and positive results with the Bactident-Oxidase strips. Catalase reaction was positive when tested by adding a drop of freshly prepared 3 % H2O2 onto bacterial colonies on agar plates and observing bubble formation.
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. FAMEs were identified using the MIDI aerobic library (TSBA, version 1.06, MIDI Inc., Newark, DE, USA). Peak identification was verified using an HP 6890 gas chromatograph equipped with mass selective detector and NIST mass spectral library. A dendrogram was constructed with the hierarchical clustering function (Euclidian distance, Ward linkage) using SYSTAT 10 for Windows software (SPSS). As the results of genetic and physiological analyses as well as cellular lipids showed that the four strains were nearly identical, cellular lipids, polyamine pattern and quinone content were analysed only for strain MT1T. Polyamine patterns were extracted and analysed according to Busse & Auling (1988) and Busse et al. (1997). The quinone system and polar lipids were determined by HPLC and two-dimensional TLC, respectively, as described by Tindall (1990a, b) and Altenburger et al. (1996).
Chromosomal DNA was purified using proteinase K, SDS and bead-beating for cell lysis, phenol/chlorophenol extractions and 2-propanol precipitation as described by Tiirola et al. (2002). The DNA base composition was determined by a direct HPLC method (Mesbah et al., 1989). 16S rRNA gene sequences were analysed as described by Männistö et al. (2001). Sequence similarities were calculated using the program BESTFIT of the GCG program package (Genetics Computer Group). Multiple alignment of the sequences was created using CLUSTAL X (Thompson et al., 1994) and edited using SEAVIEW (Galtier et al., 1996). Clustering analyses with neighbour-joining, maximum-likelihood and maximum-parsimony methods were calculated using the program PHYLO_WIN (Galtier et al., 1996) using bootstrap values based on 1000 replicates (the results are available as Supplementary Figs A–C in IJSEM Online).
All four strains, MT1T, MT101, MT103 and MT104, shared identical 16S rRNA gene sequences. Identical genomic restriction fragment length polymorphism patterns, determined by Tiirola et al. (2002), also confirmed the high degree of relatedness of the strains. The different tree constructions of the 16S rRNA gene sequences using neighbour-joining, maximum-likelihood and maximum-parsimony methods indicated that N. hassiacum DSM 14552T was the closest relative of MT1T and the MT1-like strains. Neighbour-joining analysis located N. tardaugens JCM 11434T in the same phylogenetic branch, but with low bootstrap values (36 %), indicating only low confidence. The 16S rRNA gene sequence similarity of MT1T to N. hassiacum DSM 14552T, N. aromaticivorans SMCC F199T and N. subterraneum SMCC B0478T was 96·5 %, and compared to N. tardaugens JCM 11434T it was 96·0 %. 16S rRNA gene sequence similarity values to the other type strains of the genus Novosphingobium varied between 95·1 and 96·3 %. The G+C content of the genomic DNA of MT1T was 66 mol%, which is in accordance with that described for Novosphingobium (62–67 %; Takeuchi et al., 2001). In addition, the characteristic 16S rRNA gene sequence signatures described for the genus Novosphingobium (Takeuchi et al., 2001) are present at positions 52 : 359 (C : G), 134 (G), 593 (U), 987 : 1218 (G : C) and 990 : 1215 (U : A).
The quinone system (major compound Q-10) of MT1T is in agreement with those of the species of Sphingomonadaceae and the predominant compound spermidine clearly separates MT1T from the genus Sphingomonas sensu stricto (Busse et al., 1999; Takeuchi et al., 2001). The dominant fatty acids of MT1T and the three MT1-like strains were 18 : 17c (39·1–40·7 %) and 16 : 17c (34·0–35·3 %) (fatty acid results and a cluster analysis dendrogram are available as Supplementary Table A and Fig. D). The only hydroxy fatty acid was 2-OH 14 : 0 (2-hydroxy myristic acid) (12·0–13·1 %). Other fatty acids present in significant proportions were 16 : 0 (7·0–7·8 %) and 11-methyl 18 : 17c (2·8–3·5 %). Cluster analysis of the FAME compositions revealed that MT1T, the three MT1-like strains and Novosphingobium reference strains fell into three main clusters with Euclidian distances <10. N. hassiacum DSM 14552T clustered together with MT1T and the three MT1-like strains and these strains were separated clearly from the other Novosphingobium strains. MT1T and the three MT1-like strains differed, however, from N. hassiacum by the absence of heptadecenoic acids (17 : 16c and 17 : 18c) and 2-hydroxy pentadecanoic acid (2-OH 15 : 0). The complex polar lipid profile of MT1T (Supplementary Fig. E) showed an overall similarity to other species of the genus Novosphingobium. However, the combined presence of the unknown hydrophilic lipids phospholipid PLx1 (probably identical to the hydrophilic PL reported for N. hassiacum), glycolipid GL2 (probably identical to GL2 reported for several Novosphingobium species) and the unknown phosphoglycolipid PGLx, together with minor amounts of phoshatidyldimethylethanolamine and major amounts of phosphatidylcholine, clearly distinguished MT1T from other species of Novosphingobium, including N. aromaticivorans, N. capsulatum, N. stygium, N. subterraneum, N. subarcticum and N. rosa (Busse et al., 1999) as well as N. hassiacum (Kämpfer et al., 2002).
The main physiological and biochemical features that were determined to separate Sphingomonas sensu stricto, Sphingobium, Novosphingobium and Sphingopyxis by Takeuchi et al. (2001) were hydroxy fatty acid profiles, polyamine patterns and nitrate reduction. Members of the clusters Sphingobium and Novosphingobium contain 2-OH 14 : 0 as the only 2-hydroxy fatty acid when grown in R medium (Takeuchi et al., 2001), but, as stated by the authors and described in the study of Yabuuchi et al. (2002), cultivation in different media can yield other 2-hydroxy fatty acids. Nitrate reduction was only typical in the Sphingomonas and Novosphingobium clusters. The polyamine pattern in Sphingomonas sensu stricto consists of the major compound sym-homospermidine, whereas the Novosphingobium, Sphingobium and Sphingopyxis clusters lack sym-homospermidine but contain the predominant compound spermidine. The biochemical and chemotaxonomic analyses thus support the phylogenetic evidence that the four strains MT1T, MT101, MT103 and MT104 belong to the Novosphingobium cluster, having 2-OH 14 : 0 as the major component of 2-hydroxy fatty acids, activity for nitrate reductase and spermidine as the major polyamine. However, the phenotypic markers detected for the other strains of the Novosphingobium cluster by Takeuchi et al. (2001) do not completely match our MT1-like strains, as they do not hydrolyse aesculin and do not show 
-galactosidase activity. Three other recently described Novosphingobium species, N. hassiacum, N. tardaugens and N. pentaromaticivorans, were also negative in respect of -galactosidase activity. In addition, N. tardaugens, N. hassiacum and N. capsulatum gave negative results in our aesculin hydrolysis tests. Overall, the three MT1-like strains did not assimilate any substrates tested in this study, possibly due to their highly specialized adaptation to polychlorophenols as the main carbon source. MT1T and the three MT1-like strains shared most of their physiological characteristics with N. tardaugens, but could be separated based on several characteristics (Table 1
). Furthermore, similarity between the 16S rRNA gene sequences of N. tardaugens JCM 11434T and MT1T and the three MT1-like strains was only 96·0 %.
Description of Novosphingobium lentum sp. nov.
Novosphingobium lentum (len'tum. L. neut. adj. lentum slow, pertaining to the limited growth capacity of the organism).
Cells are Gram-negative rods with rounded ends, 0·3–0·5x0·6–1·5 µm in size. Cell division is symmetric. Cells are non-sporulating and non-motile, and no flagellum is detected. Visible pale-yellow colonies are formed in 6–7 days at 22 °C on R2A agar. Colonies are smooth, shiny, flat and semi-translucent or dry, elevated and rubbery. Doubling time of the strains in R2A broth at 22 °C varies between 6·7 and 7·4 h, corresponding to 0·14–0·15 doublings h–1. Psychrotolerant. Growth is observed at 4 and 33 °C, but not at 35 °C; optimum growth at 23 °C. No growth on TSA or half-strength TSA. Catalase test is positive. Oxidase test is variable depending on the test reagents. -Galactosidase and aesculin tests are negative. Nitrate is reduced to nitrite. Hydrolysis of L-alanine p-nitroanilide and p-nitrophenol -D-glucopyranoside is detected. Major cellular fatty acids are 18 : 17c, 16 : 17c, 2-OH 14 : 0 (as the only hydroxy fatty acid), 16 : 0 and 11-methyl 18 : 17c. Contains spermidine as the only polyamide [26·4 µmol (g dry weight)–1] and contains predominantly ubiquinone-10 (99 %). Ubiquinone Q-9 is detected in trace amounts (1 %). The major polar lipids are phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, phosphatidylcholine and sphingoglycolipid. Moderate amounts of phosphatidylmonomethylethanolamine, phosphatidyldimethylethanolamine, an unknown phospholipid, an unknown phosphoglycolipid and an unknown polar lipid, and minor amounts of another phospholipid and a glycolipid are detected. The DNA G+C content of strain MT1T is 66 mol%. The 16S rRNA gene sequence of the strain matches the specific nucleotide signatures defined for the genus Novosphingobium by Takeuchi et al. (2001).
The type strain, MT1T (=DSM 13663T=CCUG 45847T), was isolated from a fluidized-bed bioreactor treating polychlorophenol-contaminated groundwater in Kärkölä, Finland.
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ACKNOWLEDGEMENTS |
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