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Actinoplanes Missouriensis 431T (= NBRC 102363T)

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Actinoplanes Missouriensis 431T (= NBRC 102363T) Standards in Genomic Sciences (2012) 7:294-303 DOI:10.4056/sigs.3196539 Complete genome sequence of the motile actinomycete T T Actinoplanes missouriensis 431 (= NBRC 102363 ) Hideki Yamamura1, Yasuo Ohnishi2, Jun Ishikawa3, Natsuko Ichikawa4, Haruo Ikeda5, Mitsuo Sekine4, Takeshi Harada4, Sueharu Horinouchi2†, Misa Otoguro1, 6, Tomohiko Tamura6, Ken-ichiro Suzuki6, Yasutaka Hoshino3, Akira Arisawa7, Youji Nakagawa1, No- buyuki Fujita4 and Masayuki Hayakawa1 1Division of Applied Biological Sciences, Interdisciplinary Graduate School of Medicine and Engineering, University of Yamanashi, Yamanashi, Japan 2Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan 3Department of Bioactive Molecules, National Institute of Infectious Diseases, Tokyo, Japan 4Biological Resource Center, National Institute of Technology and Evaluation, Tokyo, Japan 5Kitasato Institute for Life Sciences, Kitasato University, Kanagawa, Japan 6Biological Resource Center, National Institute of Technology and Evaluation, Chiba, Japan 7Bioresource Laboratories, MicroBiopharm Japan Co., Ltd., Shizuoka, Japan Corresponding author: Masayuki Hayakawa ([email protected]) †Deceased July 12th, 2009 Actinoplanes missouriensis Couch 1963 is a well-characterized member of the genus Actinoplanes, which is of morphological interest because its members typically produce spo- rangia containing motile spores. The sporangiospores are motile by means of flagella and ex- hibit chemotactic properties. It is of further interest that members of Actinoplanes are prolific sources of novel antibiotics, enzymes, and other bioactive compounds. Here, we describe the features of A. missouriensis 431T, together with the complete genome sequence and annota- tion. The 8,773,466 bp genome contains 8,125 protein-coding and 79 RNA genes. Keywords: motile actinomycetes, sporangia, zoospores, motile spores, flagellation, aerobic, Gram-positive, Micromonosporaceae, Actinoplanes, A. missouriensis Introduction Strain 431T [= NBRC 102363T = DSM 43046T = of the genus Actinoplanes, including A. ATCC 14538T and other culture collections] is the missouriensis, produce a variety of antibiotics, en- type strain of the species Actinoplanes zymes and other bioactive compounds [9-12], the missouriensis [1,2], which is a well-characterized genomes of Actinoplanes species are potentially member of the genus Actinoplanes [3]. The genus useful genetic resources for discovering secondary is of morphological interest because its members metabolites and enzymes. The genome analysis of typically produce spherical, subspherical, cylindri- the acarbose producer Actinoplanes sp. SE50/110 cal, or very irregular sporangia arising from vege- was most recently reported [13]. tative mycelia [1,4]. Sporangiospores, which are Here, we present a summary classification and a released following the immersion of sporangia in set of features for A. missouriensis strain 431T, to- water, are motile by means of polar or gether with a description of the complete genome peritrichous flagella [5] and display a positive sequencing and annotation. chemotactic response to a number of amino acids, aromatic compounds, sugars and inorganic ions Classification and features [6,7]. Recently, the flagellin gene of various A. missouriensis strain 431T was originally isolated Actinoplanes strains was successfully amplified from barnyard soil near Hamilton, Missouri, USA and sequenced to reveal the evolutionary rela- using the pollen-baiting technique and was first tionships between flagellar genes [8]. As members The Genomic Standards Consortium Yamamura et al. described by Couch in 1963 [1]. Couch also isolat- are identical (one sequence differed by 4 nucleo- ed additional strains of A. missouriensis from ten tides), but differ by 55 nucleotides (3.8%) from soil collections obtained from the Mississippi Val- the previously published 16S rRNA gene sequence ley to the West Coast. The range of 16S rRNA gene of NBRC 13243T (AB037008). The differences be- sequence similarities between strain 431T (= tween the genome data and the reported 16S NBRC 102363T) (AB711914) and valid members rRNA gene sequence are likely due to sequencing of the genus Actinoplanes was 95.7–97.9%. The errors in the previously reported sequence data. highest sequence similarities were to Actinoplanes The 16S rRNA sequence of strain 431T did not utahensis NBRC 13244T. match significantly with any 16S rRNA gene se- Figure 1 shows the phylogenetic neighborhood of quences from environmental genomic samples A. missouriensis 431T in a 16S rRNA gene-based and surveys available at the NCBI BLAST server tree. The sequences of five of the six 16S rRNA (March 2012). gene copies in the genome of A. missouriensis 431T Actinoplanes auranticolor (U58526) 0.005 Actinoplanes lobatus (AB037006) Actinoplanes sichuanensis (EU531458) Actinoplanes xinjiangensis (EU531457) Actinoplanes campanulatus (AB036995) 74 Actinoplanes capillaceus (AB013495) Actinoplanes philippinensis (D85474) Actinoplanes utahensis (AB037012) Actinoplanes sp. SE50/110 (155657-157161)** Actinoplanes missouriensis (AB711914)** Actinoplanes ianthinogenes (AB047495) 99 Actinoplanes octamycinicus (AB047494) Actinoplanes palleronii (AB037009) 99 Actinoplanes cyaneus (X93186) 51 Actinoplanes liguriensis (AJ865471) Actinoplanes rectilineatus (AB037010) Actinoplanes couchii (AM400230) 65 Actinoplanes italicus (AB048217) Actinoplanes regularis (X93188) Actinoplanes teichomyceticus (AB047513) Actinoplanes digitatis (AB037000) 56 Actinoplanes consettensis (AB048214) 100 Actinoplanes humidus (AB037004) Actinoplanes deccanensis (AB036998) Actinoplanes atraurantiacus (HQ839788) 99 Actinoplanes globisporus (AB048219)* Actinoplanes rishiriensis (AB048219) 66 Actinoplanes abujensis (HQ157185) Actinoplanes brasiliensis (X93185) Actinoplanes durhamensis (AB048215) Actinoplanes ferrugineus (AB037002) Actinoplanes tereljensis (AB468944) 86 Actinoplanes toevensis (AB468943) Dactylosporangium aurantiacum (X93191) Figure 1. Phylogenetic tree highlighting the position of A. missouriensis 431T relative to Actinoplanes sp. strain SE50/110 and other type strains within the genus Actinoplanes. The tree was inferred from 1,351 aligned characters [14,15] of the 16S rRNA gene sequence under the maximum likelihood criterion [16] and rooted with the type strain of the neighboring genus Dactylosporangium. Only bootstrap values above 50% are shown (1,000 resamplings) at branching points. Lineages with type strain genome sequencing projects registered in GOLD [17] are labeled with an asterisk, those also listed as 'Complete and Published' with two asterisks. http://standardsingenomics.org 295 Actinoplanes missouriensis 431T The color of the substrate mycelia of strain 431T is but not myo-inositol, raffinose, cellulose, adonitol, ochraceous salmon on Czapek agar. The strain D-arabinose, D-melezitose, methyl -D-glucoside, does not form aerial mycelium. On Czapek agar, D-ribose or D-sorbitol (1%, w/v) [4,29]. Strain the strain produces a soluble pale lavender pig- 431T also utilizes p-hydroxybenzoicα acid, sodium ment [1]. Optimum growth occurs at 28°C. Strain acetate and sodium fumarate (0.1%, w/v), but not 431T produces globose spores (1-1.2 µm) ar- m-hydroxybenzoic acid, sodium succinate, ranged in irregular coils within a terminal sporan- syringic acid, or vanillin (0.1%, w/v) [4,29]. Strain gium. Sporangia are globose to subglobose in 431T degrades chitin, DNA, elastin, lecithin, RNA shape and 6 to 14 µm in diameter [Figure 2] [1]. and tyrosine (26), and also actively decomposes Sporangia release motile spores, called zoospores, natural rubber [32] and flavonoids, such as after unwrapping of the membranous sheath cov- quercetin, rutin and hesperidin [33]. Strain 431T ering sporangia (Table 1) [5]. Released zoospores produces glucose isomerase (xylose isomerase) have chemotactic properties for several substrate with a molecular weight of approximately 8,000 types, including sugars, amino acids, aromatic daltons [34] and also produces 6-alkyl-4-O- compounds and mineral ions [6,7]. Flagella of the dihydrogeranyl-2-methoxyhydroquinones as nov- zoospores consist of a 44-kDa flagellar protein el phenolic lipids [35]. Antimicrobial activity (FliC) [5] encoded by the fliC gene, which has been against Streptomyces murinus ISP 5091 is positive, applied as a molecular marker in a taxonomic but is negative against Aspergillus niger LIV 131, study of the genus Actinoplanes [8]. Strain 431T Bacillus subtilis NCIB 3610 and Staphylococcus utilizes D-xylose, L-arabinose, D-glucose, D- aureus NCTC 8532 [29]. Additional physiological fructose, D-mannose, L-rhamnose, D-mannitol, and drug susceptibility data are described in detail sucrose, mannose, dextrin, D-galactose, D-lactose, elsewhere [29]. methyl -D-glucoside and L-rhamnose (1%, w/v), β Figure 2. Scanning electron micrograph of A. missouriensis 431T. Bar interval, 10 µm. 296 Standards in Genomic Sciences Yamamura et al. Table 1. Classification and general features of A. missouriensis 431T based on the MIGS recommendations [18] MIGS ID Property Term Evidence code Domain Bacteria TAS [19] Phylum Actinobacteria TAS [20] Class Actinobacteria TAS [21] Current classification Order Actinomycetales TAS [2,21-24] Family Micromonosporaceae TAS [2,21,24-26] Genus Actinoplanes TAS [2,3,27,28] Species Actinoplanes missouriensis TAS [1,2] Type strain 431 TAS [1,2] Gram stain Not tested, likely positive NAS Cell shape Produces sporangium TAS [1] Motility Motile
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