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Sphaerosporangium Gen. Nov., a New Member of the Family Streptosporangiaceae, with Descriptions of Three New Species As Sphaerosporangium Melleum Sp

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Sphaerosporangium Gen. Nov., a New Member of the Family Streptosporangiaceae, with Descriptions of Three New Species As Sphaerosporangium Melleum Sp Actinomycetologica Copyright Ó 2007 The Society for Actinomycetes Japan Sphaerosporangium gen. nov., a new member of the family Streptosporangiaceae, with descriptions of three new species as Sphaerosporangium melleum sp. nov., Sphaerosporangium rubeum sp. nov. and Sphaerosporangium cinnabarinum sp. nov., and transfer of Streptosporangium viridialbum Nonomura and Ohara 1960 to Sphaerosporangium viridialbum comb. nov. Ismet Ara1;2Ã and Takuji Kudo1 1Microbe Division/Japan Collection of Microorganisms, RIKEN BioResource Center 2-1 Hirosawa, Wako, Saitama 351-0198, Japan 2Present address: Kitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane, Minato-ku, Tokyo 108-8641, Japan (Received Sep. 12, 2006 / Accepted Dec. 20, 2006 / Published May 18, 2007) The taxonomic status of five actinomycete strains, 3-28(8)T, 4-20(13), 3D-70(20), 5-81(36) and 3D-72(35)T, isolated from sandy soil was studied using the polyphasic approach. All isolates produced branching substrate mycelia and developed spherical spore vesicles on aerial hyphae containing non-motile spores. They contained meso-diaminopimelic acid and the N-acetyl type of peptidoglycan. The predominant menaquinones were MK-9(H4) and MK-9(H6). Madurose, mannose, ribose, galactose and glucose were Advancedetected in the whole-cell hydrolysate. The diagnostic phospholipids were phosphatidylethanolamine and ninhydrin-positive phosphoglycolipids, and iso-C16:0 and 10 methyl C17:0 were detected as the major cellular fatty acids. These morphological and chemotaxonomic data were related to those of the genus Streptosporangium in the family Streptosporangiaceae. Phylogenetic analysis based on 16S rDNA sequence data suggested that the strains belong to the family Streptosporangiaceae, but not to any known genus, and form a monophyletic clade with Streptosporangium viridialbum and ‘‘Streptosporangium cinnabarinum’’. The signature nucleotides of the members of thisView clade are different from those of any known genera of the family Streptosporangiaceae. On the basis of phylogenetic analysis and the characteristic patterns of signature nucleotides as well as the morphological and chemotaxonomic data, the genus Sphaerosporangium gen. nov. is proposed for our five isolates and the type strains of Streptosporangium viridialbum and ‘‘Streptosporangium cinnabarinum’’. DNA–DNA hybridization and phenotypic characterization indicate that ProofsT the new genus comprises four species, Sphaerosporangium melleum sp. nov. with the type strain 3-28(8) (=JCM 13064T =DSM 44954T), Sphaerosporangium rubeum sp. nov. with the type strain 3D-72(35)T (=JCM 13067T =DSM 44936T), Sphaerosporangium cinnabarinum sp. nov. (=JCM 3291 =DSM 44094) and Sphaerosporangium viridialbum comb. nov. (=JCM 3027T =DSM 43801T). INTRODUCTION III, whole-cell sugar pattern B or C, fatty acid pattern 3c, major menaquinone MK-9(III, VIII-H4,H6,H2,H0) and The family Streptosporangiaceae was described for the phospholipid type PIV. The genus Streptosporangium redefined maduromycete group1). At present, the Strepto- develops stable, branched mycelia and produces globose sporangiaceae, as amended by Stackebrandt et al.2), spore vesicles (usually 10 mm in diameter) on aerial includes the following genera: Streptosporangium3), Pla- mycelia. Sporangiospores are formed by septation of nomonospora4), Microtetraspora5), Planobispora6), Plano- coiled, unbranched hyphae within the sporangium. A tetraspora7), Herbidospora8), Microbispora9), Nonomur- comparative taxonomic study and phylogenetic analysis aea9) and Acrocarpospora10). The chemotaxonomic of Streptosporangium species indicated taxonomic hetero- properties of the genera in this family are more or less geneity of the genus Streptosporangium10,11). It was similar except for the menaquinone composition of the reported that the taxonomic position of Streptosporangium genus Herbidospora. The genera are distinguished by viridialbum and ‘‘Streptosporangium cinnabarinum’’ re- morphological features including the existence of spore mains ambiguous from the viewpoint of 16S rDNA vesicles (sporangia) and the number of spores per spore sequences10,12). vesicle or chain. Members of the family have cell wall type Five actinomycete strains that formed spherical spore ÃAuthor for correspondence: Ismet Ara. Tel & Fax: +81-3-5791-6133, E-mail: [email protected] The DDBJ accession numbers for the 16S rDNA sequences of strains 3-28(8)T, 4-20(13), 3D-70(20), 5-81(36) and 3D-72(35)T are AB208714, AB208715, AB208716, AB208717 and AB208718, respectively. 1 ACTINOMYCETOLOGICA vesicles on aerial mycelia were isolated from soil. mined by TLC as described by Staneck & Roberts21). Phylogenetic analysis based on 16S rDNA sequences Reducing sugars from whole-cell hydrolysates were ana- indicated that the isolates were distinct from previously lyzed by the HPLC method of Mikami & Ishida22). The N- described genera, but closely related to S. viridialbum and acyl group of muramic acid in peptidoglycan was deter- ‘‘ S. cinnabarinum’’. In this paper, we describe the morpho- mined by the method of Uchida & Aida23). Phospholipids in logical, physiological, chemotaxonomic and phylogenetic cells were extracted and identified by the method of characterization of strains 3-28(8)T, 4-20(13), 3D-70(20), Minnikin et al.24). Methyl esters of cellular fatty acids were 5-81(36) and 3D-72(35)T, S. viridialbum and ‘‘S. cinnabar- prepared and analyzed according to the instructions of the inum’’, and propose the new genus Sphaerosporangium Microbial Identification System (Sherlock Microbial Iden- gen. nov., with Sphaerosporangium melleum sp. nov., tification System; MIDI, Hewlett Packard, Palo Alto, CA, Sphaerosporangium rubeum sp. nov., Sphaerosporangium USA)25). Isoprenoid quinones were extracted by the method cinnabarinum sp. nov. and Sphaerosporangium viridialbum of Collins et al.26,27) and were analysed using an HPLC comb. nov. system equipped with a Cosmosil 5C18 column (4:6 Â 150 mm; Nacalai Tesque, Kyoto, Japan)28) and mass spectrom- MATERIALS AND METHODS etry (Shimadzu GCMS QP 5050). Preparation and detec- tion of methyl esters of mycolic acids were performed as Strains 3-28(8)T, 4-20(13), 3D-70(20), 5-81(36) and 3D- described by Tomiyasu29). 72(35)T were isolated from sandy soil collected at a forest- Genomic DNA extraction, PCR-mediated amplification side waterfall in Chokoria, Cox’s Bazar, Bangladesh. The of the 16S rRNA gene and sequencing of the PCR products strains were isolated using the dilution plate method with were performed as described by Nakajima et al.30). The humic acid-vitamin (HV) agar13) supplemented with cyclo- sequences were multiply aligned with selected sequences AdvanceÀ1 À1 heximide (50 mg l ), nystatin (50 mg l ) and nalidixic (Fig. 2) obtained from the GenBank/EMBL/DDBJ data- acid (20 mg lÀ1)14). After 21 days of aerobic incubation at bases using the CLUSTAL X program31). The alignment 30 C, the strains were transferred and purified on yeast was manually verified and adjusted before construction extract-malt extract agar [(medium 2 of the International of a phylogenetic tree. The phylogenetic tree constructed Streptomyces Project (ISP medium 2)], and maintained as by the neighbour-joining method32) in the PAUP program working cultures on yeast-starch agar (JCM medium no. 61) (version 4.0 b10)33) was based on a comparison of 1223 containing soluble starch, 15.0 g; yeast extract,View 4.0 g; nucleotides present in all of the strains following elimi- K2HPO4, 0.5 g; MgSO4.7H2O, 0.5 g; and agar, 15.0 g in nation of gaps and ambiguous nucleotides from the se- 1 liter of distilled water (pH 7.2). quences between positions 34 and 1491 (Escherichia coli Strains 3-28(8)T, 4-20(13), 3D-70(20), 5-81(36) and 3D- position number), and Nocardia dassonvillei was used 72(35)T were grown on tap water agar, HV agar and as an outgroup. TheProofs confidence values for branches of sucrose-nitrate agar (Waksman no. 1) at 30 C for 21 days the phylogenetic tree were determined using bootstrap and then observed by light and scanning electron micro- analyses based on 1000 re-samplings34). Signature nucleo- scope (model S-2400; Hitachi, Tokyo, Japan). Motility was tides in the 16S rRNA gene of new taxon and members of observed with a light microscope using cells grown on agar the family Streptosporangiaceae were determined after medium at 30 C for 21 days and then incubated at 28 C manual verification of the CLUSTAL X alignment of the for 30–60 min in yeast-starch broth (NYS) (JCM medium sequences, and the nucleotide positions were numbered no. 61) and ISP-2 broth. The sample for scanning electron according to the corresponding position in the 16S rRNA microscopy was prepared as described by Itoh et al.15) and sequence of E. coli35). Ara & Kudo14). For culture characterization, the isolates DNA was isolated from biomass by the method of were grown for 21 days at 30 C on various agar media as Tamaoka36) and Saito & Miura37) with minor modification described by Waksman16), Shirling & Gottlieb17) and Asano as follows: achromopeptidase crude (Wako Pure Chem- & Kawamoto18). The Colour Harmony Manual19) was used icals), N-acetylmuramidase SG (Seikagaku Kogyo) and to determine the names and designations of colony colours. lysozyme were used to lyse the cells38). Cells that failed to The temperature range and NaCl tolerance for growth were be lysed by these enzymes were freeze-dried and mechan- determined on yeast-starch agar. Utilization of carbohy- ically ground as described by Raeder & Broda39). The G+C drates as sole
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