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Taxonomic Studies on Coryneform Bacteria V J. Gen. Appl. Microbiol., 18, 417-431 (1972) TAXONOMIC STUDIES ON CORYNEFORM BACTERIA V. CLASSIFICATION OF CORYNEFORM BACTERIA KAZUHIKO YAMADA ANDKAZUO KOMAGATA' Central Research Laboratories, Ajinomoto Co., Inc., Kawasaki, Japan (Received July 3, 1972) Classification and concepts of the genera of coryneform bacteria were de- scribed on the basis of the results obtained previously. Coryneform bacteria were divided into seven groups at the generic level by the combination of mode of cell division, principal amino acid in the cell wall, the guanine- cytosine content (GC content) in DNA, and biochemical and physiological characteristics. The concepts of several genera were made clearly and a new genus Curtobacterium was proposed. The scheme for differentiation of the genera of these bacteria was presented, and problems for classification of coryneform bacteria were discussed. Aerobic, gram-positive, not acid-fast, non-spore forming,. rod-shaped bacteria are called "coryneform bacteria" as a whole, and are taxonomically classified into the genera of Corynebacterium, Microbacterium, Cellulomonas, Arthrobacter, and Brevibacterium in the system of Bergey's Manual of Deter- minative Bacteriology, 7 th edition (1). However, since the generic concepts and the interrelation of these bacteria were not clearly established, the iden- tification of this group of bacteria has been actually very difficult. In the course of taxonomic studies on coryneform bacteria, the present authors (2-5) have reported . the following results : (a) The coryneform bacteria were distinguished from the true bacteria by the mode of cell division. The former develops by the snapping or bending type of cell division, and the latter propagates by simple type of cell division. (b) The coryneform bacteria were divided into five types by the principal amino acid in the cell wall, DL- and LL-diaminopimelic acid (DAP), lysine, ornithine, and a, r-diaminobutyric acid (DAB). (c) The guanine-cytosine content (GC content) in DNA of coryneform bacteria was distributed from 51 to 78%, and a specific range of GC content which characterizes the genus was not found, Present Address : The Institute of Applied Microbiology, University of Tokyo, Hongo, Tokyo. 417 418 YAMADAand KOMAGATA VOL. 18 except in Cellulomonas. (d) The coryneform bacteria were classified into seven groups by the combination of the principal amino acid in the cell wall and the morphological, cultural, biochemical, and physiological characteristics. In this paper, classification and concepts of the genera of coryneform bacteria are discussed on the basis of all the results obtained by the present authors. MATERIALS AND METHODS Microorganisms and experimental results : Microorganisms and experimental results described in the previous papers (2-5) were used. The names of strains from culture collections were used according to their designations. RESULTS AND DISCUSSION I. Grouping of coryneform bacteria In the preceding work ( 5), coryneform bacteria was divided into seven groups on the basis of the combination of the principal amino acid in the cell wall, and the morphological, cultural, biochemical, and physiological characteristics. This grouping shows an interesting relation to the mode of cell division (2) and GC content in DNA (3) as illustrated in Fig. 1. Numbers in the figure are the same as those of the grouping reported in the preceding paper (5). Bacteria of Group 1 containing DL-DAP in their cell wall as the principal amino acid grew by snapping type of cell division and their GC content gave a rather wide range from 51 to 70%. Strains of Group 2 possessing DL-DAP in their cell wall were distinguished from Group 1 by hydrolysis of gelatin and extracellular DNase activity. They grew by bending type of cell division and their GC content ranged from 61 to 63%. All the microorganisms of Group 3 containing lysine in the cell wall grew by bending type of cell di- vision and their GC content was distributed continuously from 58 to 66%. Bacteria of Group 4 possessing ornithine in the cell wall produced acid strongly and rapidly from almost all of sugars tested. They grew by bending type of cell division and their GC content fell to about 73%. Organisms of Group 5 having ornithine in the cell wall differed from Group 4 by weak and slow acid production from a limited number of sugars. They propagated by bending type of cell division and GC content ranged from 65 to 70%. Strains of Group 6 containing LL-DAP in the cell wall exhibited bending type of cell division, and their GC content was restricted to a rather narrow range from 69 to 71%. Microorganisms of Group 7 having DAB in the cell wall developed by bending type of cell division, and their GC content fell into the range from 65 to 69%. Each group placed in a box as illustrated in Fig. 1 showed taxonomic 1972 Classification of Coryneform Bacteria 419 Fig. 1. Grouping of coryneform bacteria. interests at the generic level. The properties to differentiate these seven groups are shown in Table 1. II. Taxonomic position of the seven groups 1) Group 1. Bacteria of this group propagate by snapping type of cell division and contain DL-DAP in the cell wall. The GC content of this group is distributed widely from 51 to 70%. The bacteria are strongly gram-positive and non-motile. They exhibit metachromatic granules but do not show distinctive pleomorphism. Elongated and branching cells frequently appear in the media containing 2% sodium citrate. They neither hydrolyze gelatin nor show the activity of extracellular DNase. The patterns of acid production from sugars and of assimilation of organic acids are not so specific for this group. The members with a low GC content assimilate citrate but those with a high GC content do not. The latter exhibit smaller cell form and a small number of diminutive metachromatic granules. Although GC content of this group varied widely, no difference is observed in morpholog- ical, cultural, biochemical, and physiological characteristics, mode of cell division, and type of cell wall. Therefore, these bacteria seem to be included in the same group. 420 YAMADA and KOMAGATA VOL. 18 Table 1. Characteristics to differentiate The characteristics of this group agree well with the original de- scription of Corynebacterium proposed by LEHMANN and NEUMANN (6), especially in respect to the snapping type of cell division, no motility, and the presence of metachromatic granules. Further, many strains labeled as Corynebacterium, for example, Corynebacterium diphtheriae ATCC 11913, Cor- ynebacterium equi ATCC 6939, Corynebacterium xerosis ATCC 373, etc., are included in this group. From these facts, Group 1 is regarded as the genus Corynebacterium. All the so-called glutamic acid-producing bacteria tested such as Corynebacterium callunae NRRL B-2244, Corynebacterium herculis ATCC 13868, Corynebacterium lilium NRRL B-2243, Brevibacterium divaricatum NRRL B-2312, Brevibacterium flavum ATCC 14067, Brevibacterium lactofermentum ATCC 13655 and ATCC 13869, and Micrococcus glutamicus ATCC 13032 are included in this group. VELDKAMP et al. (7) reported that the so-called glutamic acid-producing bacteria should be named Arthrobacter globi formic on the basis of their definite life cycle, cell size, and growth on synthetic media, but the present authors do not support their proposal from the present results and consideration made here. LEHMANN and NEUMANN defined that the species of Corynebacterium are non-motile and pathogenic or at least parasitic to animals. After their pro- posal, HONING (8), KISSKALT and BEREND (9), TOPPING (10), and JENSEN (11) added morphologically similar motile, plant pathogenic or soil habitat 1972 Classification of Coryneform Bacteria 421 species in the genus Corynebacterium. From the results obtained by the pre- sent authors, the strains originating from soil or plant materials such as M.. glutamicus ATCC 13032 or B. flavum ATCC 14067 were included in this group, but all the motile species or plant pathogenic species except Corynebacterium fascians were excluded from Group 1. Therefore, Corynebacteriurn should be followed fundamentally to the original description established by LEHMANN and NEUMANN, but the characteristics of pathogenicity or parasitism to ani- mals do not seem to be critical for the identification of this genus. From the results obtained and the consideration mentioned above, the following strains belong to the genus Corynebacteriurn : C. callunae AJ 1518 (NRRL B-2244), C. diphtheriae AJ 1414 (ATCC 11913), C, equi AJ 1372, AJ 1376, AJ 1378, AJ 1402 (ATCC 6939*), AJ 1403 (ATCC 10146), C. fascians AJ 1373, AJ 1398 (ATCC 12974*), C, herculis AJ 1543 (ATCC 13868), Corynebac- terium hoagii AJ 1374, AJ 1408 (ATCC 7005), C, lilium AJ 1517 (NRRL B- 2243), Corynebacterium renale AJ 1411 (ATCC 10848), C, xerosis AJ 1375 (ATCC 373), AJ 1395 (ATCC 7094), AJ 1396 (ATCC 7711), Brevibacterium ammonia- genes AJ 1443 (ATCC 6871*), AJ 1444 (ATCC 6872), AJ 1483 (IFM AU-39), B, divaricatum AJ 1498 (NRRL B-2312), B. flavum AJ 1510 (ATCC 14067), B. lactofermentum AJ 1511 (ATCC 13869), AJ 1514 (ATCC 13655), Brevibacterium * Asterisks indicate the type strain of the species. 422 YAMADAand KOMAGATA VOL. 18 linens AJ 1473 (IFM SC-84), AJ 1475 (IFM AM-17), AJ 1484 (IFM AM-27), Brevibacterium marls AJ 1480 (IFM S-30), Brevibacteriurn stationis AJ 1541 (ATCC 14403*), Brevibacterium vitarumen AJ 1525 (ATCC 10234), Microbacterium flavum AJ 1415 (ATCC 10340*), M. glutamicus AJ 1502 (ATCC 13032), and unidentified coryneform bacteria of AJ 1490, AJ 1548, AJ 1549, AJ 1562, and AJ 1958. 2 ) Groin 2. Bacteria of this group grow by bending type of cell divi- sion and have DL-DAP in the cell wall. GC content in DNA ranges from 61 to 63%. The organisms are strongly gram-positive and non-motile, and do not have metachromatic granules. Pleomorphism is not distinctive. Effect of sodium citrate on cell morphology is not so clear. They hydrolyze gelatin, show the activity of extracellular DNase, and do not produce acid from any sugars tested.
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