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DSMZ – Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Inhoffenstrasse 7b, D-38124 Braunschweig, Germany
Correspondence
Sylvie Cousin
sylvie.cousin{at}dsmz.de
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7c, iso-C15 : 0 2-OH or both); C16 : 15c, C16 : 0, iso-C15 : 0 3-OH, C16 : 0 3-OH and iso-C17 : 0 3-OH were present in smaller amounts. The major isoprenoid quinone was menaquinone 7. With one exception, binary similarity values of the almost complete 16S rRNA gene sequences determined among the isolates as well as between the isolates and type strains of Pedobacter species were lower than 98.5 %. The only exception was the close relationship between Pedobacter caeni DSM 16990T and strain WB 2.3-45T (99.2 % similarity). DNA–DNA reassociation values determined for this pair of strains was 29.8 %, indicating that strain WB 2.3-45T represents a unique genospecies. Phylogenetic analysis based on 16S rRNA gene sequences indicated that strains WB 2.1-25T and WB 2.3-71T form a group that is moderately related to P. caeni and strain WB 2.3-45T (98.5 % similarity). Strains WB 3.3-3T and WB 3.3-22T (98.5 % similarity) branched separately from these four organisms. The five phylogenetically isolated strains differed from each other as well as from the type strain of the type species (Pedobacter heparinus DSM 2366T) and some related representatives of the genus in several metabolic reactions and cultural parameters. On the basis of phenotypic and phylogenetic distinctiveness, five novel species are proposed: Pedobacter duraquae sp. nov., with WB 2.1-25T (=DSM 19034T=CIP 109481T) as the type strain; Pedobacter westerhofensis sp. nov., with WB 3.3-22T (=DSM 19036T=CIP 109479T) as the type strain; Pedobacter metabolipauper sp. nov., with WB 2.3-71T (=DSM 19035T=CIP 109480T) as the type strain; Pedobacter hartonius sp. nov., with WB 3.3-3T (=DSM 19033T=CIP 109468T) as the type strain; and Pedobacter steynii sp. nov., with WB 2.3-45T (=DSM 19110T=CIP 109507T) as the type strain.
A table showing antibiotic sensitivities of the Pedobacter WB isolates is available as supplementary material with the online version of this paper.
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) was established to accommodate Sphingobacterium heparinum (Takeuchi & Yokota, 1992) and some other heparinolytic bacteria that, on the basis of DNA–DNA hybridization (Steyn et al., 1992, 1993), were shown to fall outside the realm of the genus Sphingobacterium. Several novel species have been added to the genus Pedobacter during the past few years, isolated mainly from soil (Ten et al., 2006; Yoon et al., 2007), freshwater (Gallego et al., 2006; Hwang et al., 2006; Vanparys et al., 2005) and glaciers (Margesin et al., 2003; Shivaji et al., 2005). During a recent survey on the microbial composition of a hard-water creek, almost 1000 strains were isolated on R2A agar, about 50 % of which had swarming (40 %) or slime-producing (10 %) capacities. Whereas almost all of the swarming bacteria and many slime-formers could be affiliated to the genus Flavobacterium (Brambilla et al., 2007; Cousin et al., 2007), other slime-producing organisms were members of different proteobacterial taxa (Stackebrandt et al., 2007; unpublished data) and of the phylum Bacteroidetes (unpublished data). Among the latter organisms, five strains, identified by partial 16S rRNA gene sequences as members of the genus Pedobacter, were subjected to a polyphasic taxonomic study; subsequently, all were described as representatives of novel species.
The isolation of strains from the Westerhöfer Bach on medium R2A (Difco) has been described by Brambilla et al. (2007). Strains WB 2.1-25T, WB 2.3-71T and WB 2.3-45T were isolated about 180 m downstream of the spring (station 2; station 1 being the source of Westerhöfer Bach), whereas strains WB 3.3-3T and WB 3.3-22T were isolated about 250 m downstream of the spring (station 3). Following isolation, strains were transferred and maintained on medium 67 (M67; DSMZ, 2001) at 25 °C for several days. The same medium was also used to cultivate the reference strains Pedobacter heparinus DSM 2366T, Pedobacter africanus DSM 12126T, Pedobacter caeni DSM 16990T and Pedobacter cryoconitis DSM 14825T. Maintenance in glycerol served as a medium-term preservation method. Cultures were preserved in liquid N2 and freeze-dried.
DNA extraction and PCR amplification of the 16S rRNA genes were carried out as described by Rainey et al. (1996). The PCR amplificons were purified by using the QIAquick PCR Purification kit (QIAGEN) according to the instructions of the manufacturer. Sequencing of the PCR products, manual alignment of the sequences with those of Pedobacter type strains and determination of similarity coefficients were done as described by Rainey et al. (1996). The algorithm of De Soete (1983) and the neighbour-joining algorithm (Felsenstein, 1993) were used to generate tree topologies.
Binary similarity values of the almost complete sequences of the 16S rRNA gene, determined for the five WB strains, were lower than 98.5 %. Two strain clusters emerged from the analysis, one containing strains WB 2.1-25T, WB 2.3-71T and WB 2.3-45T (97.7–98.5 % similarity) and the other containing strains WB 3.3-3T and WB 3.3-22T (98.5 % similarity). The similarity values between the two groups were 95.8–97.0 %. With the exception of P. caeni DSM 16990T, which shared a 16S rRNA gene sequence similarity value of 99.2 % with strain WB 2.3-45T, the type strains of other Pedobacter species were more distantly related to the isolates (91.5–98.2 % similarity). P. caeni DSM 16990T, P. africanus DSM 12126T and P. cryoconitis DSM 14825T were included in the following studies because they showed the highest similarity values with the novel WB strains. P. heparinus DSM 2366T was included as the type strain of the type species of the genus. Phylogenetic relationships of the novel strains to other Pedobacter species type strains are shown in a phylogenetic tree (Fig. 1) generated based on the algorithm of De Soete (1983). Topologies of the neighbour-joining and maximum-likelihood trees differed slightly in the branching points of the deeply branching clades (not shown), but the affiliation of phylogenetic neighbours are in accord with those published previously (Gallego et al., 2006; Margesin et al., 2003; Shivaji et al., 2005; Ten et al., 2006; Yoon et al. 2007).
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); however, values above this threshold value are not necessarily indicative of novel genospecies. Therefore, the genomic relatedness between P. caeni 16990T and WB 2.3-45T was determined by using the spectrophotometric DNA–DNA reassociation method. DNA was isolated using a French pressure cell (Thermo Spectronic) and was purified by hydroxyapatite chromatography as described by Cashion et al. (1977). DNA–DNA hybridization was carried out as described by De Ley et al. (1970), with the modifications of Huß et al. (1983) and Escara & Hutton (1980), using a model Cary 100 Bio UV/VIS-spectrophotometer equipped with a Peltier-thermostatted 6x6 multicell changer and a temperature controller with in situ temperature probe (Varian). Two reassociation experiments resulted in 35.7 and 23.9 % reassociation (mean of 29.8 %). These low values indicate that strain WB 2.3-45T represents a novel genospecies.
The novel strains and some Pedobacter reference strains were subjected to fatty acid methyl ester analysis to confirm membership to the genus. Cultures of all strains were grown on trypticase soy agar (TSA; Difco) for 24 h. Fatty acids were extracted and analysed (Miller, 1982) according to the standard protocol of the Microbial Identification System (MIS; MIDI Microbial ID). Extracts were analysed using a Hewlett Packard model HP6890A GC equipped with an FID as described by Kämpfer & Kroppenstedt (1996). The major fatty acids were summed feature 3 (C16 : 17c, iso-C15 : 0 2-OH or both) (35–48 % of total) and iso-C15 : 0 (15–26.5 %); C16 : 15c, C16 : 0, iso-C15 : 0 3-OH, C16 : 0 3-OH and iso-C17 : 0 3-OH were present in smaller amounts. The amounts of fatty acids determined in the analysed reference strains agreed by and large with the values indicated in the literature (e.g. Steyn et al., 1998; Gallego et al., 2006). A dendrogram of fatty acid relationships is shown in Fig. 2. Although most strains differed in the quantities of their fatty acids only, the separation of P. heparinus DSM 2366T and P. africanus DSM 12126T from P. cryoconitis DSM 14825T, P. caeni DSM 16990T and the WB strains is in accord with the 16S rRNA gene tree (Fig. 1
), as is the position of strain WB 2.3-45T adjacent to the type strain of P. caeni. Menaquinones were determined according to Minnikin et al. (1984). MK-7 was the major peak (97–100 %) in all strains tested.
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and the species description. All strains were grown on R2A medium. Strains WB 2.1-25T, WB 2.3-45T, WB 2.3-71T, WB 3.3-22T, P. africanus DSM 12126T, P. caeni DSM 16990T and P. heparinus DSM 2366T were grown at 25 °C, whereas strain WB 3.3-3T and P. cryoconitis DSM 14825T were grown at 20 °C. Growth was measured by reading the OD at 600 nm. The temperature optimum was tested over a period of 3–6 days using a temperature gradient incubator model TN-3 (Toyo Kagaku Sangyo) at 1–36 °C in steps of 2 °C. The optimal pH for growth was tested in buffered M67 at 25 °C at pH 4.0–9.5 in steps of 0.2 pH units using three different buffer solutions (Na2HPO4/NaH2PO4, succinic acid/NaOH and 2-amino-2-methyl-1,3-propanediol/HCl). Analysis was done at 1 day intervals over a period of 6 days. Salt tolerance was tested on R2A medium supplemented with 1–10 % NaCl in steps of 2 %.
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). Cells were tested for gliding movement by the hanging drop method as described by Bernardet et al. (2002); motility was tested with cells from 2-day-old liquid cultures on soft agar incubated for 3 days at 23 °C. The presence of flexirubin pigments (Bernardet et al., 2002), Gram-stain using the aminopeptidase and KOH reactions, catalase activity (H2O2 test) and heparin hydrolysis (Zimmermann et al., 1990) were also tested. Cytochrome c oxidase was determined by adding a few drops of tetramethyl-p-phenylenediamine solution to a 3-day-old slant of each strain. All WB isolates were aerophilic and microaerophilic under the conditions provided in a candle jar, non-gliding and motile.
Antimicrobial susceptibilities were determined with the disc diffusion method using a ST6090 Disc Dispenser (Oxoid). Isolates were classified into three categories (sensitive, resistant and intermediate) based on the quantitative interpretation criteria recommended by the NCCLS (2000). All strains studied were resistant to cefalotin (30 µg), cefotaxime (30 µg), oxacillin (5 µg), mezlocillin (30 µg), aztreonam (30 µg), gentamicin (10 µg), colistin (10 µg), vancomycin (30 µg), amikacin (30 µg), polymyxin B (300 IU), kanamycin (30 µg) and neomycin (30 µg); all were sensitive to doxycycline (30 µg), imipenem (10 µg) and tetracycline (30 µg). Results in which the WB strains differ from each other are presented in Supplementary Table S1 available in IJSEM Online.
Enzymic activities and carbon assimilation tests were determined using the commercial API ZYM, API 50 CH and API 20NE systems (bioMérieux) and the utilization or oxidization of carbon sources was determined using the GN MicroPlate system (Biolog) according to the instructions of the manufacturers. A modified AUX media (Somvanchi et al., 2006) with 0.6 g MgSO4 . 7H2O instead of 6 g was used for strain WB 2.1-25T. API ZYM tests were read after 6 h incubation, whereas API 50 CH, API 20NE and GN MicroPlate tests were read after 48 h. Incubation was at 25 °C except for P. cryoconitis DSM 14825T and strain WB 3.3-3T, which were inoculated at 20 °C. Results are included in the species descriptions and Table 1.
Many of the reactions indicated as positive for all strains of the genus Pedobacter also scored positive in our tests (Table 1). Some other substrates were used by the majority of strains, i.e. D-xylose, sucrose, gentiobiose and salicin. The occurrence of reactions scored as ‘weak’, however, somehow hinders a clear-cut interpretation of inter-strain similarities at the level of physiological reactions. In several tests recorded, P. heparinus DSM 2366T showed an unexpectedly significant number of reactions that deviated from those indicated in the original description (Steyn et al., 1998). In its negative reaction towards the API and Biolog substrates, strain DSM 2366T was similar to strain WB 2.3-71T. Of the reactions listed in Table 1, these two strains do not have a single positive score in common, although both of them share between two and four positive scores with other representatives. Except for P. heparinus DSM 2366T and P. africanus DSM 12126T, none of the strains investigated were heparinase-positive. The presence of phenotypic differences observed among the isolates confirms their distinct phylogenetic position determined by 16S rRNA gene sequence analysis and, where done, by DNA–DNA reassociation experiments. It is concluded that the five WB isolates each represents a novel species in the genus Pedobacter; descriptions are given below.
Description of Pedobacter duraquae sp. nov.
Pedobacter duraquae (dur.a'quae. L. adj. durus, -a, -um hard; L. fem. n. aqua water; N.L. gen. fem. n. duraquae from/of hard water).
Gram-negative rods, 1.9–2.5x0.63–0.83 µm, motile and non-spore-forming. Grows at 9–32 °C; optimum growth at 25–27 °C. Grows at pH 5.70–8.15. Weak growth in 4 % NaCl. Colonies on R2A, TSA and NA media are circular, butyrous, opaque, smooth, entire and non-pigmented. Colonies are ivory white and convex (0.1 mm in diameter) on R2A, sand yellow (0.4 mm in diameter) and raised on TSA, and translucent and flat (0.2 mm in diameter) on NA. Microaerophilic. Hydrolyses DNA. Positive for valine arylamidase, 
-glucuronidase, 
-glucosidase and -glucosidase and weak for esterase (C4) and chymotrypsin (API ZYM). Positive for amygdalin, D-arabinose, D-ribose, D-xylose, D-adonitol, gentiobiose, inulin, L-rhamnose, salicin, D-fructose, D-galactose, sucrose and D-raffinose (API 50 CH and API 20NE). Positive for -cyclodextrin and dextrin and negative for D-raffinose (Biolog). Additional reactions are listed in Table 1 and Supplementary Table S1.
The type strain, WB 2.1-25T (=DSM 19034T=CIP 109481T), was isolated from a site about 180 m downstream of the spring of the Westerhöfer Bach, Westerhof, 40 km north of Göttingen, Germany (5 ° 45' 49'' N 1 ° 05' 31.7'' E).
Description of Pedobacter hartonius sp. nov.
Pedobacter hartonius (har.to'ni.us. M.L. masc. n. Harto the Harz, a mountain range in northern Germany; N.L. masc. adj. hartonius pertaining to the Harz).
Gram-negative rods, 1.5–2.5x0.63–0.83 µm, motile and non-spore-forming. Grows at 6–26 °C; optimum growth at 12–16 °C. Grows at pH 5.7–7.8 and in 4 % NaCl. Colonies on R2A, TSA and NA media are circular, butyrous, convex, opaque, smooth, entire and non-pigmented. Colonies are pearl white (0.1 mm in diameter) on R2A and sand yellow (0.4 mm in diameter) and ivory white (0.1 mm in diameter) on TSA and NA, respectively. Microaerophilic. Hydrolyses gelatin. Positive for -glucosidase and weak for esterase (C4) and -glucosidase (API ZYM). Positive for amygdalin, D-arabitol, D-xylose, gentiobiose, L-rhamnose, salicin, N-acetyl-D-glucosamine, D-fructose, D-mannitol and D-galactose (API 50 CH and API 20NE). Positive for methyl -D-glucoside and -D-lactose, weak reactions with dextrin, L-arabinose and lactulose, and negative for D-mannitol (Biolog). Additional reactions are listed in Table 1 and Supplementary Table S1.
The type strain, WB 3.3-3T (=DSM 19033T=CIP 109468T), was isolated from a site about 250 m downstream of the spring of the Westerhöfer Bach, Westerhof, 40 km north of Göttingen, Germany (5 ° 45' 49'' N 1 ° 05' 31.7'' E).
Description of Pedobacter metabolipauper sp. nov.
Pedobacter metabolipauper [me.ta'bo.li.pau'per. N.L. n. metabolismus metabolism (word stem metabol-); L. masc. adj. pauper poor; N.L. masc. adj. metabolipauper metabolically poor].
Gram-negative rods, 1.7–2.7x0.83 µm, motile and non-spore-forming. Grows at 8–31 °C; optimum growth at 24–26 °C. Grows at pH 5.9–8.0. No growth in 4 % NaCl. No growth on TSA. Colonies on R2A and NA media are 0.1 mm in diameter, ivory white, circular, butyrous, raised, opaque, smooth and entire. Colonies are non-pigmented. Microaerophilic. Hydrolyses DNA weakly. Positive for trypsin and -glucosidase and weak for esterase (C4) and chymotrypsin (API ZYM). Positive for gentiobiose, methyl -D-mannopyranoside and sucrose (API 50 CH and API 20NE). Negative for sucrose (Biolog). Additional reactions are listed in Table 1 and Supplementary Table S1.
The type strain, WB 2.3-71T (=DSM 19035T=CIP 109480T), was isolated from a site about 180 m downstream of the spring of the Westerhöfer Bach, Westerhof, 40 km north of Göttingen, Germany (5 ° 45' 49'' N 1 ° 05' 31.7'' E).
Description of Pedobacter westerhofensis sp. nov.
Pedobacter westerhofensis (wes.ter.ho.fen'sis. N.L. masc. adj. westerhofensis pertaining to Westerhof, a village in the Harz Mountains).
Gram-negative rods, 1.7–2.5x0.83–1.0 µm, motile and non-spore-forming. Grows at 9–28 °C; optimum growth at 22–24 °C. Grows at pH 5.3–7.8. No growth in 4 % NaCl. Colonies on R2A, TSA and NA media are 0.1–0.2 mm in diameter, pearl white, circular, butyrous, convex, opaque, smooth and entire. Colonies are non-pigmented. Microaerophilic. Hydrolyses gelatin. Hydrolyses DNA weakly. Positive for -glucosidase and -glucosidase (API ZYM). Positive for D-xylose, gentiobiose, L-rhamnose, methyl -D-mannopyranoside, D-galactose, sucrose and D-raffinose and weak reactions with N-acetyl-D-glucosamine (API 50 CH and API 20NE). Positive for dextrin, -D-lactose, lactulose, methyl -D-glucoside and L-serine, weak reactions with -cyclodextrin, L-arabinose, psicose and L-threonine, and negative for D-raffinose (Biolog). Additional reactions are listed in Table 1 and Supplementary Table S1.
The type strain, WB 3.3-22T (=DSM 19036T=CIP 109479T), was isolated from a site about 250 m downstream of the spring of the Westerhöfer Bach, Westerhof, 40 km north of Göttingen, Germany (5 ° 45' 49'' N 1 ° 05' 31.7'' E).
Description of Pedobacter steynii sp. nov.
Pedobacter steynii (stey'ni.i. N.L. gen. masc. n. steynii of/from Steyn, named after P. L. Steyn, the microbiologist who described the genus Pedobacter).
Gram-negative rods, 1.70–3.75x0.83 µm, motile and non-spore-forming. Grows at 10–30 °C; optimum growth at 25–27 °C. Grows at pH 5.70–8.45. Weak growth in 4 % NaCl. Colonies on R2A, TSA and NA media are circular, butyrous, convex (raised on NA), opaque, smooth, entire, non-pigmented and slimy. Colonies are 0.4 mm in diameter and pearl white on R2A, and 0.2 mm in diameter and ivory white on TSA and NA media. Microaerophilic. Hydrolyses casein, DNA and gelatin. Positive for esterase (C4), valine arylamidase and -glucosidase (API ZYM). Positive for protease gelatin, D-xylose, gentiobiose, salicin, D-galactose, N-acetyl-D-glucosamine, D-raffinose, glycerol and glycogen (API 50 CH and API 20NE). Positive for -cyclodextrin, dextrin, -D-lactose, methyl -D-glucoside, L-glutamic acid, L-serine and L-threonine, weak reactions with D-glucuronic acid and succinic acid, and negative for D-raffinose (Biolog). Additional reactions are listed in Table 1 and Supplementary Table S1.
The type strain, WB 2.3-45T (=DSM 19110T=CIP 109507T), was isolated from a site about 180 m downstream of the spring of the Westerhöfer Bach, Westerhof, 40 km north of Göttingen, Germany (5 ° 45' 49'' N 1 ° 05' 31.7'' E).
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ACKNOWLEDGEMENTS |
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Z. Ali, S. Cousin, A. Fruhling, E. Brambilla, P. Schumann, Y. Yang, and E. Stackebrandt Flavobacterium rivuli sp. nov., Flavobacterium subsaxonicum sp. nov., Flavobacterium swingsii sp. nov. and Flavobacterium reichenbachii sp. nov., isolated from a hard water rivulet Int J Syst Evol Microbiol, October 1, 2009; 59(10): 2610 - 2617. [Abstract] [Full Text] [PDF]
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H.-Y. Weon, B.-Y. Kim, C.-M. Lee, S.-B. Hong, Y.-A. Jeon, B.-S. Koo, and S.-W. Kwon Solitalea koreensis gen. nov., sp. nov. and the reclassification of [Flexibacter] canadensis as Solitalea canadensis comb. nov. Int J Syst Evol Microbiol, August 1, 2009; 59(8): 1969 - 1975. [Abstract] [Full Text] [PDF]
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N. S. Gordon, A. Valenzuela, S. M. Adams, P. W. Ramsey, J. L. Pollock, W. E. Holben, and J. E. Gannon Pedobacter nyackensis sp. nov., Pedobacter alluvionis sp. nov. and Pedobacter borealis sp. nov., isolated from Montana flood-plain sediment and forest soil Int J Syst Evol Microbiol, July 1, 2009; 59(7): 1720 - 1726. [Abstract] [Full Text] [PDF]
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-aminobutyric acid, urocanic acid, inosine, uridine, thymidine, phenylethylamine, putrescine, 2-aminoethanol, 2,3-butanediol, glucose 6-phosphate, methyl