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1 Hans-Knöll-Institut für Naturstoff-Forschung eV, D-07745 Jena, Germany
2 School of Biology, University of Newcastle, Newcastle upon Tyne NE1 7RU, UK
3 Rheinische Friedrich-Wilhelms-Universität, Institut für Pharmazeutische Biologie, D-53115 Bonn, Germany
Correspondence
Michael Goodfellow
m.goodfellow{at}ncl.ac.uk
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains HKI 0315T, HKI 0316, HKI 0189T, HKI 0314T, HKI 0186T and HKI 0190T are AY442263–AY442268, respectively.
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emend. Kim et al. 2003. The genus Kitasatospora (formerly Kitasatosporia) was proposed by 
mura et al. (1982) and currently includes aerobic, Gram-positive, non-motile, chemo-organotrophic actinomycetes that form an extensively branched substrate mycelium, aerial hyphae that differentiate into long chains of spores, contain N-acetylated muramic acid, major proportions of diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides (phospholipid type 2 sensu Lechevalier et al., 1977), predominant amounts of hexahydrogenated menaquinones with nine isoprene units, fatty acids with major amounts of iso and anteiso components and whole-organism hydrolysates that are typically rich in galactose, and in LL- and meso-diaminopimelic acid (meso-A2pm). Aerial spores on solid culture and submerged spores in liquid media contain LL-A2pm whereas mycelia grown under both cultural conditions have mainly meso-A2pm (mura et al., 1981, 1982; Takahashi et al., 1984; Groth et al., 2003).
The 13 species of Kitasatospora that have validly published names at the time of writing are Kitasatospora azatica (Nakagaito et al. 1993) Zhang et al. 1997, Kitasatospora cheerisanensis Chung et al. 1999, Kitasatospora cineracea Tajima et al. 2001, Kitasatospora cochleata (Nakagaito et al. 1993) Zhang et al. 1997, Kitasatospora cystarginea Kusakabe and Isono 1992, Kitasatospora griseola Takahashi et al. 1985, Kitasatospora kifunensis (Nakagaito et al. 1993) Groth et al. 2003, Kitasatospora mediocidica Labeda 1988, Kitasatospora niigatensis Tajima et al. 2001, Kitasatospora paracochleata (Nakagaito et al. 1993) Zhang et al. 1997, Kitasatospora phosalacinea Takahashi et al. 1985, Kitasatospora putterlickiae Groth et al. 2003 and Kitasatospora setae mura et al. 1983 [species name corrected by mura et al. (1985)]; K. setae is the type species of the genus. Members of these species form a distinct phyletic line in the 16S rRNA gene tree and can be delineated using a combination of genotypic and phenotypic data (Nakagaito et al., 1992a, b; Groth et al., 2003).
Six out of 18 Kitasatospora strains isolated from soil samples collected from several geographical locations during a study designed to improve the isolation and rapid differentiation of kitasatosporae from phylogenetically similar streptomycetes were the subject of a polyphasic taxonomic study. This showed that five of the six strains should be recognized as novel species. Strains HKI 0315T (=2148-013T), HKI 0316 (=2122-022) and HKI 0314T (=2050-015T) were isolated from soil samples collected in Kumagura and Kyoto, Japan, and in Gansu Province, China, respectively, using PY-BHI agar (Yokota et al., 1993) and a standard dilution plate procedure; these isolates were originally misclassified as streptomycetes. Strains HKI 0190T (=2292-041T), HKI 0186T (=2293-012T) and HKI 0189T (=2291-120T) were isolated from rhizosphere soil of Maytenus plants in Brazil using either PY-BHI agar (strains HKI 0186T and HKI 0190T) or yeast extract/starch agar (Kudo et al., 1993) (strain HKI 0189T) and a phage-assisted isolation method.
The phage-assisted isolation method involved heating air-dried soil (1 g) at 80 °C in a dry oven for 1 h, making a soil suspension in 10 ml aqueous sodium pyrophosphate (0·2 % w/v), mixing on a rotary shaker for 30 min, and allowing the soil particles to settle prior to decanting the supernatant, which was kept at 4 °C. The soil fraction was treated with the same amount of solvent and the resultant preparation was ultrasonicated for 5 min at 50 W. The second supernatant was added to the first, the combined preparation was diluted and 0·1 ml aliquots of the various dilutions were spread over casein mineral (Altenburger et al., 1996), humic acid (Hayakawa & Nonomura, 1987), PY-BHI agar (Yokota et al., 1993) and yeast extract starch agar isolation plates, which were carefully overlaid with 100 µl per plate of a high titre suspension (about 108–109 plaque-forming units) of polyvalent Streptomyces phage S7 (DSM 49153) and incubated at 28 °C for up to 4 weeks. Colonies that exhibited a Streptomyces-like morphology were transferred to oatmeal agar plates (ISP medium 3; Shirling & Gottlieb, 1966) and incubated for further growth. These isolates were checked again for their susceptibility to Streptomyces phage S7 as described below. All S7-resistant strains were grown on organic medium 79 (Prauser et al., 1987) and oatmeal agar, which favour the growth of vegetative mycelium (contains meso-A2pm) and spores (contain LL-A2pm), respectively. Strains found to contain both of these isomers were studied further.
Biomass for the chemotaxonomic analyses of the six isolates and marker strains of K. azatica (DSM 41650T), K. kifunensis (DSM 41654T), K. mediocidica (DSM 43929T), K. phosalacinea (DSM 43860T) and K. putterlickiae (DSM 44665T) was prepared by cultivating them for 24–48 h at 28 °C in liquid organic medium 79 and bacto-tryptic soy broth (Sigma-Aldrich). The strains were grown on ISP media 2, 3, 4 and 5 (Difco; Shirling & Gottlieb, 1966) at 28 °C for up to 21 days, after which cultural and morphological properties were recorded; morphological features were observed by light and electron microscopy. The dimensions of the spores were measured by using an Axioskop 2 microscope equipped with image-analysing AXIO VISION 2.05 software (both from Zero). Samples for electron microscopy were prepared from heavily sporulating cultures grown on ISP medium 3 following Shirling & Gottlieb (1966) and observed by using a Zeiss EM 902A electron microscope at an acceleration voltage of 80 kV.
Physiological tests were carried out as described by Groth et al. (2003). Susceptibility to most of the tested antibiotics was examined by placing antibiotic discs (Difco) on organic medium 79 agar plates that were seeded with suspensions of the test strains grown in a soft agar layer for up to 2 days at 28 °C. Nalidixic acid and novobiocin were added to ISP 2 agar plates, which were then seeded with spores of the strains. Susceptibility to polyvalent Streptomyces phages was tested by dropping high-titre suspensions of phage S7 (DSM 49153) onto agar plates seeded with spores of the test strains held in a soft agar layer; the phage was propagated as described by Groth et al. (2003). Standard procedures were used to determine the isomers of A2pm in whole-organism hydrolysates (Rhuland et al., 1955; Hasegawa et al., 1983), type of muramic acid (Uchida & Aida, 1984) and presence of mycolic acids (Minnikin et al., 1975), together with whole-organism fatty acid (MIDI system; Agilent), menaquinone (Collins et al., 1977), polar lipid (Minnikin et al., 1979; Collins & Jones, 1980) and sugar profiles (Becker et al., 1965; Saddler et al., 1991).
16S rRNA gene sequence amplification and analysis of strains HKI 0186T, HKI 0189T and HKI 0190T were carried out as described by Edwards et al. (1989), and of strains HKI 0314T, HKI 0315T and HKI 0316 as described by Kim et al. (1998). The resultant sequences were aligned manually with corresponding almost complete sequences of representatives of most actinomycete genera; in each case reference sequences were retrieved from DDBJ/EMBL/GenBank. Phylogenetic analysis was carried out using the least-squares (Fitch & Margoliash, 1967), maximum-likelihood (Felsenstein, 1981) and neighbour-joining (Saitou & Nei, 1987) tree-making algorithms from the PHYLIP 3.5c package (Felsenstein, 1993). Evolutionary distance matrices for the neighbour-joining method were generated according to the model of Jukes & Cantor (1969). The stability of the resultant unrooted tree topologies were evaluated by carrying out bootstrap analyses (Felsenstein, 1985) of the neighbour-joining data based on 1000 resamplings, using the SEQBOOT and CONSENSE options from the PHYLIP 3.5c software.
DNA was extracted from the strains included in the DNA–DNA relatedness studies using a French pressure cell (Thermo Spectronic) and then purified by chromatography on hydroxyapatite as described by Cashion et al. (1977). DNA–DNA hybridizations were carried out in 2x SSC and DMSO (10 %, v/v) at 70 °C, using modifications (Escara & Hutton, 1980; Huß et al., 1983) of the procedure described by De Ley et al. (1970) and a model 2600 spectrophotometer equipped with a model 2527-R thermoprogrammer and plotter (Gilford Instrument Laboratories). Renaturation rates were computed using the TRANSFER.BAS program of Jahnke (1992).
Preliminary phylogenetic analysis of the almost complete 16S rRNA gene sequences of the six isolates (1368–1444 nt) placed them within the evolutionary radiation occupied by the genus Kitasatospora (data not shown). The isolates were aerobic, Gram-positive, non-motile, formed non-fragmenting, extensively branched substrate mycelia, aerial hyphae that differentiated into long chains of smooth-surfaced spores (Fig. 1) and grew well on ISP media (Table 1) and within the pH range 5·0–9·5. They were also characterized by the presence of N-acetylated muramic acid, galactose, predominant proportions of hexahydrogenated menaquinones with nine isoprene units, major amounts of diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides, LL- and meso-A2pm in whole-organism hydrolysates and contained varying proportions of iso- and anteiso-branched, straight-chain and unsaturated fatty acids (Table 2) but lacked mycolic acids. The isolates were resistant to polyvalent Streptomyces phage S7. All of these properties are consistent with their classification in the genus Kitasatospora (mura et al., 1982; Zhang et al., 1997). This phenotypic profile also serves to distinguish the isolates from members of the genera Streptacidiphilus and Streptomyces (Kim et al., 2003a). The isolates were sensitive to low concentrations of novobiocin (5 µg ml–1) and hence are unlikely to grow on the novobiocin-containing agar medium used by Tajima et al. (2001) to isolate K. cineracea and K. niigatensis strains.
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that the six isolates are scattered throughout the Kitasatospora 16S rRNA gene sequence tree. The closest relationship between any of the isolates is between strain HKI 0316 and K. kifunensis NBRC 15206T. This relationship is supported by all three tree-making algorithms and by a bootstrap value of 77 % in the neighbour-joining analysis. The two strains share a 16S rRNA gene sequence similarity of 99·6 %, which corresponds to 6 nt differences over 1365 locations. However, they have a DNA–DNA relatedness of 78 %, a value well above the 70 % cut-off point recommended for the delineation of genomic species (Wayne et al., 1987). The two strains also share key phenotypic properties, notably the ability to form short cylindrical, smooth-surfaced spores in straight to spiral spore chains (rectiflexibiles to spirales), to produce melanin pigments on tyrosine agar, to hydrolyse starch, to produce 
-galactosidase, 
-glucosidase, -mannosidase and naphthol-AS-BI phosphohydrolase, to use (+)-D-mannitol and (+)-D-sucrose as sole carbon sources and to grow in the presence of NaCl (2·5 %, w/v), lincomycin hydrochloride (2 µg), penicillin G (10 IU) and polymyxin B (300 IU). In contrast, neither of the organisms is able to liquefy gelatin, peptonize milk, reduce nitrate, grow on (+)-D-raffinose or (+)-L-rhamnose as sole carbon sources or to produce -glucosidase or N-acetyl--glucosamidase. The two strains have a fatty acid profile rich in C16 : 0, anteiso-C15 : 0 and iso-C15 : 0 components. These data are consistent with the assignment of isolate HKI 0316 (=2122-022) to K. kifunensis (Nakagaito et al. 1993) Groth et al. 2003.
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); they share 16S rRNA gene sequence similarities with this organism of 98·5 and 99·0 %, respectively, values equivalent to 15 and 14 nt differences at 1430 locations. However, the two isolates are more closely related to one another, having a 16S rRNA gene sequence similarity of 99·2 %, which corresponds to 12 nt differences at 1444 sites, but clearly belong to distinct genomic species as they share a DNA–DNA relatedness of 40·1 %. It is also evident from Tables 2 and 3 that these organisms can be distinguished using a broad range of phenotypic properties. These data indicate that isolates HKI 0190T and HKI 0186T form novel centres of taxonomic variation in the genus Kitasatospora for which the names Kitasatospora paranensis sp. nov. and Kitasatospora terrestris sp. nov. are proposed.
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). This is exemplified in the present study by isolates HKI 0190T and HKI 0186T. It is evident from Tables 2 and 3 that isolate HKI 0315T can be distinguished from K. kifunensis DSM 41654T using several phenotypic properties. It is clear that isolate HKI 0315T merits species status in the genus Kitasatospora; the name proposed for this novel taxon is Kitasatospora nipponensis sp. nov.
The relatively close phylogenetic relationship found between isolate HKI 0314T and K. mediocidica NBRC 14789T is supported by the results from all of the tree-making algorithms and by a bootstrap value of 90 % in the neighbour-joining analysis (Fig. 2). The two organisms share a 16S rRNA gene sequence similarity of 98·7 %, a value equivalent to 19 nt differences at 1429 sites. The two strains can be separated readily using a combination of phenotypic properties (Table 3). It is proposed that isolate HKI 0314T be recognized as a novel Kitasatospora species, for which the name Kitasatospora gansuensis sp. nov. is proposed.
The final isolate, strain HKI 0189T, forms a distinct phyletic line at the foot of the 16S rRNA Kitasatospora gene sequence tree (Fig. 2). This organism is most closely related to K. phosalacinea; the two organisms share a 16S rRNA gene sequence similarity of 98·7 %, a value corresponding to 19 nt differences at 1423 locations. However, strain HKI 0189T can be distinguished from K. phosalacinea using several phenotypic properties (Table 3). It is apparent from these data that isolate HKI 0189T forms a novel centre of taxonomic variation in the genus Kitasatospora, for which the name Kitasatospora arboriphila sp. nov. is proposed.
Description of Kitasatospora arboriphila sp. nov.
Kitasatospora arboriphila (ar.bo.ri.phi'la. L. n. arbor a tree; Gr. adj. philos loving, N.L. fem. adj. arboriphila tree loving).
Aerobic, Gram-positive, non-acid-fast actinomycete that produces a yellowish brown to dark brown or olive substrate mycelium and a grey to dark grey aerial spore mass on glycerol/asparagine, inorganic salts/starch, oatmeal and yeast extract/malt extract agars. Soluble pigments are not formed, but melanoid pigments are produced on peptone/yeast extract/iron and tyrosine agars. Spore chains are long, straight to spiral with hooks and loops with 20 or more cylindrical, smooth-surfaced spores (1·1–1·7x1·3–2·4 µm) per chain (Fig. 1a). Submerged spores are formed sparsely in liquid culture. Temperature range for growth is 15–40 °C (optimum 28–32 °C); growth does not occur at 10 °C or above 40 °C. pH range for good growth is pH 5·0–8·0; growth does not occur at either pH 4·5 or pH 9·0. Additional phenotypic properties are given in Table 3. The cell wall contains meso- and LL-A2pm; the muramic acid moiety is N-acetylated. Whole-organism hydrolysates contain galactose, mannose, glucose and ribose. The major polar lipids are phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides. The predominant fatty acids are iso-C16 : 0 (25 %), iso-C15 : 0 (17 %) and anteiso-C15 : 0 (12 %); mycolic acids are absent. The major menaquinones are MK-9(H6) (49 %) and MK-9(H8) (28 %).
The type and only strain is HKI 0189T (=2291-120T=DSM 44785T=NCIMB 13973T), which was isolated from a soil sample collected from the roots of the tree Maytenus aquifolia in Ribeirao Preto, Brazil.
Description of Kitasatospora gansuensis sp. nov.
Kitasatospora gansuensis (gan.su.en'sis. N.L. fem. adj. gansuensis pertaining to Gansu, a province in China, the origin of the soil from which the type strain was isolated).
Aerobic, Gram-positive, non-acid-fast actinomycete that produces a yellowish- or orange–brown to dark-brown substrate mycelium and a white to beige aerial spore mass on glycerol/asparagine, inorganic salts/starch, oatmeal and yeast extract/malt extract agars; soluble pigments are not formed on these media but melanoid pigments are produced on peptone/yeast extract/iron and tyrosine agars. Spore chains are long, straight to flexuous, with 20 or more cylindrical, smooth-surfaced spores (0·8–1·3x1·6–3·0 µm) per chain (Fig. 1b). Submerged spores and irregular fragments are formed in liquid culture. Temperature range for growth is 6–32 °C (optimum 25–28 °C); growth does not occur below 6 °C or at 35 °C. pH range for good growth is pH 5·0–9·5; growth does not occur at pH 4·5 or above pH 9·5. Additional phenotypic properties are given in Table 3. The cell wall contains meso- and LL-A2pm; the muramic acid moiety is N-acetylated and whole-organism hydrolysates contain galactose, ribose, mannose and rhamnose. The polar lipids are phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol, phosphatidylinositol mannosides and an unknown glycolipid. The predominant fatty acids are anteiso-C15 : 0 (21 %), C16 : 0 (19 %), iso-C15 : 0 (10 %) and iso-C16 : 0 (10 %); mycolic acids are absent. The major menaquinone is MK-9(H6) (75 %).
The type and only strain is HKI 0314T (=2050-015T=DSM 44786T=NCIMB 13974T), which was isolated from a sample of forest soil collected in the Lianhua Shan Reservation, Gansu Province, China.
Description of Kitasatospora nipponensis sp. nov.
Kitasatospora nipponensis (nip.pon.en'sis. N.L. fem. adj. nipponensis pertaining to Nippon, the native name for Japan, the origin of the soil from which the type strain was isolated).
Aerobic, Gram-positive, non-acid-fast actinomycete that produces a yellowish- or reddish-brown substrate mycelium and a grey aerial spore mass on glycerol/asparagine, inorganic salts/starch, oatmeal and yeast extract/malt extract agars. A purple soluble pigment is formed on oatmeal agar, but melanoid pigments are not produced on peptone/yeast extract/iron and tyrosine agars. Spore chains are open spirals, long straight loops and hooks with 20 or more cylindrical, smooth-surfaced spores (1·1–1·6x1·2–2·3 µm) per chain (Fig. 1c). Submerged spores are formed in liquid culture. Temperature range for growth is 10–32 °C (optimum 25–28 °C); growth does not occur at 6 °C or at 37 °C. pH range for good growth is pH 5·0–8·0; growth does not occur at pH 4·5 or above pH 8·5. Additional phenotypic properties are given in Table 3. The cell wall contains meso- and LL-A2pm; the muramic acid moiety is N-acetylated and whole-organism hydrolysates contain galactose, mannose, ribose and glucose. The major polar lipids are phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol, phosphatidylinositol mannosides and an unknown phospholipid. The predominant fatty acids are iso-C16 : 0 (38 %) and iso-C15 : 0 (10 %); mycolic acids are absent. The major menaquinone is MK-9(H6) (74 %).
The type and only strain is HKI 0315T (=2148-013T=DSM 44787T=NCIMB 13975T), which was isolated from a soil sample collected at Kumagura, Japan.
Description of Kitasatospora paranensis sp. nov.
Kitasatospora paranensis (pa.ra.nen'sis. N.L. fem. adj. paranensis pertaining to Parana, a state of Brazil, the origin of the soil from which the type strain was isolated).
Aerobic, Gram-positive, non-acid-fast actinomycete that produces a yellowish-brown to dark-brown substrate mycelium and a grey aerial spore mass on glycerol-asparagine, inorganic salts/starch, oatmeal and yeast extract/malt extract agars. Soluble pigments are not formed, but melanoid pigments are produced on peptone/yeast extract/iron and tyrosine agars. Spore chains are long straight to flexuous with 20 or more cylindrical, smooth-surfaced spores (1·1–1·4x1·2–2·1 µm) per chain (Fig. 1d). Submerged spores are rarely formed in liquid culture. Temperature range for growth is 10–37 °C (optimum 25–28 °C); growth does not occur at 6 °C or at 40 °C. pH range for good growth is pH 5·0–9·0; growth does not occur at either pH 4·0 or pH 9·5. Additional phenotypic properties are given in Table 3. The cell wall contains both meso- and LL-A2pm; the muramic acid moiety is N-acetylated and whole-organism hydrolysates contain galactose, mannose and glucose. The polar lipids are phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol mannosides, phosphatidylserine and an unknown phospholipid. The predominant fatty acids are iso-C16 : 0 (19 %), anteiso-C15 : 0 (16 %) and C16 : 0 (14 %); mycolic acids are absent. The major menaquinone is MK-9(H6) (53 %) with minor components MK-9(H4) (22 %) and MK-9(H2) (14 %).
The type and only strain is HKI 0190T (=2292-041T=DSM 44788T=NCIMB 13976T), which was isolated from rhizosphere soil of Maytenus ilicifolia, Contenda, Parana State, Brazil.
Description of Kitasatospora terrestris sp. nov.
Kitasatospora terrestris (ter.res'tris. L. fem. adj. terrestris of the earth, terrestrial).
Aerobic, Gram-positive, non-acid-fast actinomycete that produces a yellowish-brown to dark-brown or greyish-brown substrate mycelium and a grey aerial spore mass on glycerol/asparagine, inorganic salts/starch, oatmeal and yeast extract/malt extract agars. Soluble pigments are not formed. The formation of melanoid pigments is weak on peptone/yeast extract/iron and tyrosine agars. Spore chains are straight, hooked and spiral with 20 or more cylindrical, smooth-surfaced spores (1·1–1·5x1·3–2·8 µm) per chain (Fig. 1e). Submerged spores are formed in liquid culture. Temperature range for growth is 15–40 °C (optimum 28–32 °C); growth does not occur at 10 °C or at 42 °C. pH range for good growth is pH 5·0–9·0; growth does not occur at pH 4·5 or at pH 9·5. Additional phenotypic properties are shown in Table 3. The cell wall contains meso- and LL-A2pm; the muramic acid moiety is N-acetylated and whole-organism hydrolysates contain galactose, mannose and glucose. The polar lipids are phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol (traces), phosphatidylinositol, phosphatidylinositol mannosides, phosphatidylserine and an unknown glycolipid. The predominant fatty acids are iso-C16 : 0 (21 %), iso-C15 : 0 (16 %) and anteiso-C15 : 0 (10 %); mycolic acids are absent. The major menaquinone is MK-9(H6) (76 %).
The type and only strain is HKI 0186T (=2293-012T=DSM 44789T=NCIMB 13977T), which was isolated from a soil sample of the roots of Maytenus aquifolia, Ribeirao Preto, Brazil.
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ACKNOWLEDGEMENTS |
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