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The Genus Arthrobacter Was Established for Soil Coryneform Bacteria with a Life Cycle Different from Corynebacterium and Mycobacterium by Connand DIM- Mickin 1947 (1)

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The Genus Arthrobacter Was Established for Soil Coryneform Bacteria with a Life Cycle Different from Corynebacterium and Mycobacterium by Connand DIM- Mickin 1947 (1) J. Gen. App!. Microbiol., 29, 59-71 (1983) PIMELOBACTER GEN. NOV., A NEW GENUS OF CORYNEFORM BACTERIA WITH LL-DIAMINOPIMELIC ACID IN THE CELL WALL KEN-ICHIRO SUZUKII AND KAZUO KOMAGATA Institute of Applied Microbiology, The University of Tokyo, Bunkyo-ku, Tokyo 113, Japan (Received December 22, 1982) Coryneform bacteria with LL-diaminopimelic acid in the cell wall were characterized. Morphological, biochemical, and chemotaxonomic char- acteristics, and DNA homologies revealed that they form an independent cluster among the coryneform bacteria. A new genus Pimelobacter is proposed for this group of coryneform bacteria. The type species of the genus Pimelobacter is Pimelobacter simplex comb. nov., which was previ- ously named Art hrobacter simplex. Further, Pimelobacter jensenii sp. nov. and Pimelobacter tumescens comb. nov. are also described. The genus Arthrobacter was established for soil coryneform bacteria with a life cycle different from Corynebacterium and Mycobacterium by CONNand DIM- MICKin 1947 (1). The chemotaxonomic heterogeneity of the genus Arthrobacter was first pointed out by CUMMINSand HARRIS(2). Some strains have lysine in the cell wall and others have LL-diaminopimelic acid (LL-DAP). Later, FIEDLER et a!. (3) and YAMADAand KoMAGATA(4) reported that a majority of the Arthro- bacter strains, including the type species Arthrobacter globiformis, have lysine and a few strains have LL-DAP in the cell wall. YAMADAand K®MAGATA(4) also reported that the DNA base composition of Arthrobacter strains with lysine in the cell wall ranges from 58 to 65 mol % of guanine plus cytosine (mol 0 G-+ C), while the DNA base composition of the cory- neform bacteria with LL-DAP in the cell wall ranges from 70 to 72 mol % G+C; but the two groups of bacteria resemble each other with respect to their mor- phological and biochemical characteristics. The study of DNA homologies show that the coryneform bacteria with LL-DAP in the cell wall fall into one cluster and 1 Present address : Japan Collection of Microorganisms , Institute of Physical and Chemical Research, Wako-shi, Saitama 351, Japan. Reprint requests to: Dr. K. Suzuki, Japan Collection of Microorganisms, Institute of Physical and Chemical Research, Wako-shi, Saitama 351, Japan. 59 60 SUZUKI and KOMAGATA VOL. 29 are clearly distinguished from Arthrobacter strains with lysine in the cell wall (S). On the other hand, PRAVSER(6) established the genus Nocardioides for the no- cardioform bacteria with LL-DAP in the cell wall and suggested a close relationship of the strains of this genus to Arthrobacter simplex, one of the coryneform bacteria with LL-DAP in the cell wall. The taxonomic position of the coryneform bacteria with LL-DAP in the cell wall (the LL-DAP coryneform bacteria) needs clarification. KEDDIEand BOUSFIELD (7) also pointed out the necessity of establishing a new genus for the group of bacteria on the basis of much more information. The present study deals with the characterization of the LL-DAP coryneform bacteria and the establishment of a new genus, Pimelobacter gen. nov. MATERIALS AND METHODS Bacterial strains. We studied the strains listed in Table 1. Art hrobacter simplex CNF 035 and Arthrobacter tumescens CNF 067 are the type strains of those species (8). They were isolated by JENSEN(9). A. simplex CNF 091 was also isolated by GUNDERSENand JENSEN(10) as a herbicide-decomposing bacterium. Two strains of "Brevibacterium lipolyticum," CN F 036 and CNF 037, were isolated by IIzUKA and KOMAGATA(11) from soils of an oil field in Japan. In addition to the five strains of the LL-DAP coryneform bacteria, six strains of Arthrobacter with lysine in the cell wall, six strains of Nocardioides albus, and the type strain of Streptomyces albus were studied. Corynebacterium diphtheriae CNF 017 (=AJ 1414=ATCC 11913) was employed as a reference for cell wall analysis, and Micrococcus luteus CNF 040 (=IAM 1056=ATCC 4698) was used as a reference for determination of DNA base composition. Names in quotation marks are not on the Approved Lists of Bacterial Names, 1980 (8). Morphological characteristics. Cell morphology was observed in the cells grown on YM agar, which contained 0.5 % Bacto-peptone (Difco), 0.3 % yeast extract (Difco), 0.3 % malt extract (Difco), 1 % glucose, and 2 % agar; and on glucose-asparagine agar (GA agar), which contained 1 % glucose, 0.5 % asparagine, and 0.5 % K2HPO4, and 2 % agar. The latter medium was used for mycelial for- mation in the strains studied. Biochemical characteristics. Extracellular DNase was tested using DNase test agar (Difco). Urease and assimilation of organic acids were examined by the methods of YAMADAand KOMAGATA(12). Assimilation of carbohydrates was tested by the method of the International Streptomyces Project (13). Cells grown on GA agar were used for inocula, except for A. tumescens CNF 067 which was grown on YM agar. Since A, tumescens requires thiamine (14), vitamins were added to the basal medium in the three procedures, N, T, and 0 as shown in Table 2. The N medium contained 10 ppm thiamine HCI, 1 ppm biotin, 10 ppm ribo- flavin, 10 ppm nicotinic acid, 10 ppm pyridoxin, and 10 ppm p-aminobenzoic acid. 1983 Pimelnhacter gen. nov. b1 Table 1. Bacterial strains studied. 62 SUZUKI and KOMACATA VOL. 29 The T medium contained 10 ppm thiamine HC1, and the 0 medium contained no nutritional additives. Principal amino acids in the cell wall. DAP isomers in the cell wall were determined by the method of STANECKand RoBERTS(15). Isoprenoid quinones. Isoprenoid quinone was analyzed by high performance liquid chromatography. The apparatus and the analytical conditions were the same as those reported by TAMAOKAet al. (16). The abbreviations used for Iso- prenoid quinones in the present study are : M K, menaquinone; MK-n with n de- noting a specified number of isoprene units in the side chain; MK-n(Hm) with m indicating the number of hydrogen atoms saturating the Isoprenoid chain. Cellular fatty acid composition. Cellular fatty acid composition was deter- mined by the method previously reported (17-19). DNA base composition and DNA homologies. DNA was extracted by the method of SAITOand MIURA(20). DNA base composition was calculated by the formula of MARMURand DOTY(21) from the melting temperature in SSC (SSC: 0.15 M NaCI and 15 mM trisodium citrate, pH 7.0). DNA of Micrococcus luteus CNF 040 (= JAM 1056, =ATCC 4698), which contains 72.0 mol % GEC, was employed as a reference for determining the DNA base composition and for the negative control of DNA hybridization. DNA homologies were carried out by the method previously reported (5,17). The hybridization temperature was 70°. RESULTS Morphological characteristics Pleomorphism occurred in the five strains of the LL-DAP coryneform bacteria (Fig. 1). The cells were irregularly rod-shaped in the early stage of growth and coccoid in old cultures. After one day of cultivation, the cells of A. simplex CNF 035 were 1.0 ,ccmthick and 1.5 to 6.0µm long (most of them were 2.0 to 3.0 ,um long). Two strains of "Brevibacterium lipolyticum" CNF 036 and CNF 037 tended to be coccoid earlier than the other LL-DAP coryneform bacteria. A. Fig. 1. Morphological changes of cells in Pimelobacter simplex CNF 091. a) 1-day culture on YM agar, b) 7-day culture on YM agar. The bar indicates 10 tam. 1983 Pimelobacter gen, nov. 63 Fig. 2. Comparison of cell morphologies in Pimelobacter simplex strains and a Nocardioides albus strain. a) P, simplex CNF 035, (b) P, simplex CNF 091, and c) N, albus CNF 146. Cells of each strain were those cultivated on YM agar at 30° for 2 days. The bar indicates 10 um. globiformis CNF 022 was also pleomorphic and the cells were 1.2 to 1.5 µm by 1.5 to 7.0 um in one-day cultures. A comparison of the cell morphology is shown in Fig. 2. Strains of N. albus had a regular filamentous form and its fragmented rods, and they were not coccoid even in the old culture. The cells were 0.5 to 0.6 µm in diameter. The motility of A, simplex CNF 035 and "Brevibacterium lipolyticum" CNF 036 and CNF 037 was observed by the hanging drop method. Flagellation of these strains was reported previously to be lateral (12,14) or peritrichous (10). A. tumescens CNF 067 and A. simplex CNF 091 were not motile. The five strains of the LL-DAP coryneform bacteria formed white, glossy, smooth, and entire colonies on YM agar. On the other hand, the colonies of N. albus were white and entire, but wrinkled. Some strains of N. albus formed aerial mycelia on GA agar. Biochemical characteristics The results of the biochemical tests are shown in Table 2. No strains produced acid from glucose. All of the LL-DAP coryneform bacteria except A. simplex CNF 091 were positive for DNase and negative for urease. Acetic acid was as- similated by all the strains studied. Citric acid was not assimilated by the four strains of the LL-DAP coryneform bacteria and by five strains of N. albus. The strains of the LL-DAP coryneform bacteria did not assimilate uric acid, while five strains of Arthrobacter with lysine in the cell wall and six strains of N. albus did so. All the strains studied grew on glucose and sucrose. A. tumescens CNF 067 re- quired thiamine for growth. Among the strains of the LL-DAP coryneform bac- teria, A. tumescens CNF 067 grew at the expense of mannitol, and A. simplex CNF 091 did so at the expense of L-rhamnose. Principal amino acids in the cell wall It was confirmed that the five strains of the LL-DAP coryneform bacteria and the type strains of N.
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