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1 Leibniz-Institut für Naturstoff-Forschung und Infektionsbiologie eV, Hans-Knöll-Institut, Beutenbergstrasse 11a, 07745 Jena, Germany
2 Division of Microbiology, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia
3 Universität Tübingen, Biologisches Institut, Auf der Morgenstelle 28, 72076 Tübingen, Germany
4 Sanofi-Aventis Deutschland GmbH, Industriepark Hoechst, 65926 Frankfurt (Main), Germany
5 Division of Biology, University of Newcastle, Newcastle upon Tyne NE1 7RU, UK
Correspondence
Ingrid Groth
Ingrid.Groth{at}hki-jena.de
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ABSTRACT |
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A dendrogram showing relationships between the isolates and between them and the type strains of closely related Amycolatopsis species based on MALDI-TOF MS data is available with the online version of this paper.
Present address: CLONDIAG Chip Technologies GmbH, Löbstedter Strasse 103-105, 07749 Jena, Germany. 
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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). The genus currently contains 34 recognized species, most of which have been described in the past five years using polyphasic taxonomic approaches (Goodfellow et al., 2001; Labeda et al., 2003; Groth et al., 2007). Members of most of these species have been isolated from geographically diverse soils (Kim et al., 2002; Saintpierre-Bonaccio et al., 2005; Lee et al., 2006; Tan et al., 2006a), and others from clinical material (Labeda et al., 2003; Huang et al., 2004), vegetable matter (Goodfellow et al., 2001) and from the wall of a hypogean Roman catacomb (Groth et al., 2007).
Amycolatopsis strains can be distinguished from members of other genera classified in the family Pseudonocardiaceae by using a combination of chemotaxonomic and morphological markers (Kim & Goodfellow, 1999) and genus-specific oligonucleotide primers based on 16S rRNA gene sequences (Tan et al., 2006b). A range of phenotypic markers can be weighted to distinguish between species with validly published names (Saintpierre-Bonaccio et al., 2005; Lee et al., 2006; Groth et al., 2007). The present polyphasic study was designed to determine the taxonomic position of three strains which had been isolated from a medieval alum slate mine. The strains were assigned to the genus Amycolatopsis on the basis of their morphological properties and ability to produce the diagnostic amplification products when probed with the genus-specific 16S rRNA oligonucleotide primers AMY2 (5'-GGTGTGGGCGACATCCACGTTGT-3') and ATOP (5'-GTATCGCAGCCCTCTGTACCAGC-3') as described by Tan et al. (2006b). The resultant data showed that the isolates represent a novel Amycolatopsis species for which the name Amycolatopsis saalfeldensis sp. nov. is proposed.
The three strains were isolated from the surfaces of acidic and heavy-metal-containing rocks of two galleries in the medieval alum slate mine Feengrotten in Saalfeld, Thuringia, Germany. Strain HKI 0457T was isolated from rock in the central grotto (second level of the mine) by touching it with a sterile cotton swab and dispersing adhering bacteria in 1 ml sterile distilled water. Aliquots of the resultant suspension were spread over casein mineral agar plates (Altenburger et al., 1996), supplemented with cycloheximide (50 µg ml–1), and incubated at 28 °C for 4 weeks. Strains HKI 0473 and HKI 0474 were isolated from rock surfaces towards the end of the Hess von Wichdorff Grotto (first level of the mine) by using the same procedure, but plating out onto humic acid agar (Hayakawa & Nonomura, 1987).
Working cultures of the isolates were maintained on organic medium 79 agar (Prauser & Falta, 1968). The cultures were preserved as mixtures of hyphae and fragmented spores in organic medium 79 broth and in glycerol medium (Groth et al., 2007) at –80 °C. Stock cultures were also kept in liquid organic medium 79 supplemented with 5 % DMSO in the vapour phase of liquid nitrogen. Biomass for the chemotaxonomic and molecular systematic studies was prepared by growing the isolates and Amycolatopsis kentuckyensis DSM 44652T, Amycolatopsis lexingtonensis DSM 44653T, A. mediterranei DSM 43304T, Amycolatopsis pretoriensis DSM 44654T, A. rifamycinica DSM 46095T and Amycolatopsis tolypomycina DSM 44544T in liquid organic medium 79 and bacto-tryptic soy broth (Sigma-Aldrich) for 24 to 48 h at 28 °C. For MALDI-TOF MS analysis the strains were cultivated as described by Groth et al. (2007).
Chromosomal DNA was extracted from the three isolates using slight modifications of the method of Pospiech & Neumann (1995). PCR amplification of 16S rRNA genes was achieved using the conserved primers 27F (5'-AGAGTTTGATCCTGGCTCAG-3') and 1522R (5'-AAGGAGGTGATCCAGCCGCA-3') (Edwards et al., 1989) and the following conditions: initial denaturation at 95 °C for 5 min, 35 cycles of 94 °C for 15 s, 55 °C for 15 s, 72 °C for 1 min; and a final extension for 10 min at 72 °C. After electrophoretic separation the 16S rRNA genes were extracted from the agarose gel using the MinElute Gel Extraction Kit (Qiagen), according to the manufacturer's instructions. Forward and reverse strands of amplified DNA fragments were directly sequenced using a Big Dye Terminator v. 3.1 Cycle Sequencing Kit and an ABI Prism 3100 sequencer (both Applied Biosystems).
The resultant 16S rRNA gene sequences were aligned manually using the PHYDIT program (http://plaza.snu.ac.kr/
jchun/phydit/), against corresponding sequences of representatives of the family Pseudonocardiaceae retrieved from the GenBank/EMBL/DDBJ databases. Unrooted phylogenetic trees were inferred using the least-squares (Fitch & Margoliash, 1967), maximum-parsimony (Fitch, 1971) and neighbour-joining (Saitou & Nei, 1987) tree-making algorithms. Evolutionary distance matrices were generated for the least-squares and neighbour-joining algorithms, using the method of Jukes & Cantor (1969). All of the phylogenetic analyses were carried out using the PHYLIP suite of programs (Felsenstein, 1993). The robustness of the resultant trees was evaluated by bootstrap analysis (Felsenstein, 1985) of neighbour-joining data based on 1000 resamplings using the TREECON program (Van de Peer & De Wachter, 1994). The root position of the tree was estimated using Prauserella rugosa DSM 43194T (accession no. AF051342) as the outgroup organism.
Almost complete 16S rRNA gene sequences were generated for the three novel isolates (>1447 nt), all of which had identical sequences. Comparison of the 16S rRNA gene sequences with corresponding sequences of representatives of the family Pseudonocardiaceae showed that the isolates belong to the genus Amycolatopsis (data not shown). The high 16S rRNA gene sequence similarities found between the isolates and representatives of the genus Amycolatopsis (94.3–98.4 %) support the addition of these strains to the genus.
It is apparent from Fig. 1 that the isolates are most closely associated with the A. mediterranei 16S rRNA subclade, though this relationship is not supported by a high bootstrap value in the neighbour-joining analysis. Strain HKI 0457T was most closely related to A. rifamycinica DSM 46095T. The two organisms shared a 16S rRNA gene sequence similarity of 98.4 %, a value that corresponded to 23 differences at 1432 locations. The isolates also shared relatively high 16S rRNA gene sequence similarities with the type strains of A. kentuckyensis (98.1 %), A. lexingtonensis (98.1 %), A. mediterranei (98.2 %), A. pretoriensis (98.2 %) and A. tolypomycina (98.1 %). DNA–DNA relatedness studies were not carried out between isolate HKI 0457T and its closest phylogenetic neighbours, as it is known that the type strains of Amycolatopsis species classified in the A. mediterranei 16S rRNA subclade share much higher 16S rRNA gene similarities than those cited above but have lower DNA–DNA relatedness values (Labeda et al., 2003; Wink et al., 2003; Bala et al., 2004), that is, values well below the 70 % cut-off point recommended for the delineation of genomic species (Wayne et al., 1987).
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), menaquinone profiles (Collins et al., 1977; Groth et al., 1996), muramic acid type (Uchida & Aida, 1984), the presence of mycolic acids (Minnikin et al., 1975), predominant whole-organism sugars (Becker et al., 1965; Schön & Groth, 2006) and polar lipid patterns (Minnikin et al., 1979; Collins & Jones, 1980), using appropriate standards. All three isolates contained meso-A2pm, arabinose and galactose in whole-organism hydrolysates (wall chemotype IV sensu; Lechevalier & Lechevalier, 1970) together with glucose, mannose and rhamnose, N-acetylated muramic acid, diphosphatidylglycerol, phosphatidylethanolamine, hydroxyphosphatidylethanolamine, phosphatidylglycerol, phosphatidylinositol, phosphatidylserine and two uncharacterized glycolipids (phospholipid pattern 2 sensu Lechevalier et al., 1977), and tetrahydrogenated menaquinones with nine isoprene units [MK-9(H4)] as the major isoprenologue (86–88 % of total) with minor proportions of MK-8(H4) (4–5 %), MK-9(H6) (1–3 %) and MK-10(H4) (2 %), but they lacked mycolic acids. These data serve to distinguish the isolates from all other wall chemotype IV actinomycetes, apart from those classified in the genus Amycolatopsis (Lechevalier et al., 1986; Kim & Goodfellow, 1999; Takahashi, 2001).
The fatty acid profiles of the isolates grown in bacto-tryptic soy broth for 48 h were determined using the MIDI system (www.midi-inc.com/). All of the strains had a very similar fatty acid composition in which 14-methylpentadecanoic acid (iso-C16 : 0) was the major component (41–42 % of total); the fatty acids found in smaller proportions were iso-C17 : 0 (8–10 %), iso-C15 : 0 (8–9 %), iso-C14 : 0 (7–9 %), iso-2OH C16 : 0 (4–6 %), C15 : 0 (6 %) and C17 : 0 (5–7 %). These profiles are similar to those recorded for members of established Amycolatopsis species (Yassin et al., 1993; Wink et al., 2004; Groth et al., 2007).
Morphological properties of the isolates were examined following growth on ISP media 2 and 3 agar plates (Difco; Shirling & Gottlieb, 1966) at 28 °C for up to 21 days. The pH growth range was established using shake flasks of liquid organic medium 79, adjusted to pH values between 4.5 and 10.0 with either 1 M HCl or 20 %, (w/v) Na2CO3 solution, and incubated for 6 days at 28 °C. The isolates were also tested for their ability to grow on solidified minimal medium (Amoroso et al., 2000) supplemented with CuSO4 (2 mM) and NiCl2 (5 mM), respectively, following growth at 28 °C for 21 days. The remaining physiological tests, including the determination of antibiotic sensitivity and enzymic activities, were carried out as described by Groth et al. (2003). The isolates formed an extensively branched substrate mycelium on the ISP media tested and moderate amounts of aerial hyphae only on ISP medium 3. Substrate and aerial hyphae fragmented into rod-like elements typical of Amycolatopsis strains. The strains also grew in the presence of copper and nickel salts, and shared a broad range of phenotypic properties. Some of the latter can be used to distinguish the isolates from the type strains of phylogenetically close Amycolatopsis species classified in the Amycolatopsis 16S rRNA gene clade (Table 1).
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. The reactions were prepared in a final volume of 10 µl containing 0.5 U GoTaq (Promega), the GoTaq flexi buffer, 0.2 mM of each of the four dNTPs, 3 mM MgCl2, 1 µM primer AS4, 2 µM primer AS15 and about 20 ng extracted DNA. For initial calculation of Tm and primer concentration, the biomath Tm-calculator provided by Promega was used (www.promega.com/biomath/calc11.htm). The different primer concentrations were empirically optimized to give the best possible size range and distribution of the resulting bands. Amplifications were performed three times using Thermo-Fast low profile PCR plates (ABgene) in an MJ research PTC 225 thermal cycler according to the following profile: an initial step at 94 °C for 2 min, 57 °C for 40 s and 72 °C for 30 s to provide templates, followed by 30 cycles at 92 °C for 20 s, 57 °C for 40 s, 72 °C for 30 s and a final extension at 72 °C for 2 min. Amplification products were separated by gel electrophoresis in native polyacrylamide gels (8 %) containing 0.5 % TBE buffer. Gels were stained with SYBR Safe (Invitrogen). Fingerprints were analysed using GelComparII software (version 4.5, Applied Maths). The banding patterns were automatically matched (optimization value 1 %, position tolerance value 0.4 %). This computed matching was refined manually afterwards. A phylogenetic clustering of the banding patterns was achieved using the built-in maximum-parsimony tree-making algorithm (Fitch, 1971). The topology of the resulting tree (Fig. 2) was evaluated by bootstrap analysis (Felsenstein, 1985) based on 1000 resamplings. It is clear from Fig. 2 that the isolates gave almost identical UP-PCR fingerprint patterns which serve to distinguish them from corresponding patterns of their closest phylogenetic neighbours.
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; Groth et al., 2007) using a Voyager mass spectrometer. The resultant spectra were added to an existing Amycolatopsis dataset, and the data were analysed using Data Explorer software (Applied Biosystems) and the peak lists compared using SARAMIS software (Anagnos Tec). It is evident from our results (supplementary Fig. S1 available with the online version of this paper) that the isolates have similar profiles that distinguish them from those of Amycolatopsis type strains, including those representing phylogenetically close taxa. It is evident from the genotypic and phenotypic data that isolates HKI 0457T, HKI 0473 and HKI 0474 form a homogeneous taxon that can be distinguished readily from representatives of phylogenetically close Amycolatopsis species classified in the A. mediterranei 16S rRNA gene clade. It is, therefore, proposed that the isolates be classified in the genus Amycolatopsis as Amycolatopsis saalfeldensis sp. nov.
Description of Amycolatopsis saalfeldensis sp. nov.
Amycolatopsis saalfeldensis (saal.feld.en'sis. N.L. fem. adj. saalfeldensis from Saalfeld, named after the place of origin, a town in Thuringia, Germany).
Aerobic, Gram-positive, non-acid/alcohol-fast, non-motile, catalase-positive actinomycete which forms an extensively branched vegetative mycelium (hyphal diameter 0.5–0.6 µm) that fragments into squarish rod-like elements. The substrate mycelium carries moderate amounts of white aerial hyphae which fragment into squarish rod-like elements. Diffusible pigments are not produced. Good growth occurs between 20 and 35 °C, but growth is not evident below 10 or at 42 °C. Grows well between pH 4.5 and 8.0 and in the presence of 2 % (w/v) NaCl, but does not grow at pH 9.0 or in the presence of 4 % (w/v) NaCl. Grows on minimal medium supplemented with NiCl2 (5 mM) and CuSO4 (2 mM), respectively. Oxidase is produced, aesculin and urea hydrolysed, and H2S produced. Nitrate is not reduced to nitrite. Degrades casein, gelatin, hippurate, Tween 80 and tyrosine, but not adenine or potato starch. L-Arabinose, D-fructose, D-glucose, meso-inositol, D-mannitol, L-rhamnose (type strain weakly), sucrose and D-xylose are used as sole carbon sources for energy and growth, but not cellulose (all at 1 %, w/v). Similarly, acetate, aconitate, benzoate (weakly), citrate and succinate are used as sole carbon and energy sources for growth, but not DL-tartrate (all at 0.2 %, w/v). Produces 
-chymotrypsin (weakly), leucine arylamidase, esterase (C4), esterase lipase (C8), N-acetyl-
-glucosamidase, -glucosidase, naphthhol-AS-BI-phosphohydrolase, acid phosphatase and alkaline phosphatase, but not -galactosidase, -glucuronidase, lipase (C14), -mannosidase or trypsin (API ZYM tests). Susceptible to chloramphenicol (30 µg per disc), ciprofloxacin (5 µg per disc, weakly), imipenem (10 µg per disc), kanamycin sulphate (30 µg per disc), lincomycin hydrochloride (2 µg per disc, weakly), ofloxacin (10 µg per disc, weakly), oxytetracycline hydrochloride (30 µg per disc), rifampicin (30 µg per disc), streptomycin sulfate (10 µg per disc) and vancomycin hydrochloride (30 µg per disc), but is resistant to ampicillin (10 µg per disc), methicillin (5 µg per disc), norfloxacin (10 µg per disc), novobiocin (5 µg per disc), penicillin G (10 IU per disc) and polymyxin B (300 IU per disc). Additional phenotypic properties are shown in Table 1
. Chemotaxonomic characters are typical for Amycolatopsis species.
The type strain, HKI 0457T (=DSM 44493T=NRRL B-24474T), was isolated from the surface of rocks in a medieval alum slate mine.
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ACKNOWLEDGEMENTS |
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