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The Patterns Produced by Nine Enzymes of Ballistosporogenous Yeasts and Supposedly Related Yeasts Were Studied by Electrophoresis on Poly- Acrylamide Gel

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The Patterns Produced by Nine Enzymes of Ballistosporogenous Yeasts and Supposedly Related Yeasts Were Studied by Electrophoresis on Poly- Acrylamide Gel J. Gen. App!. Microbiol., 29, 115-143 (1983) AN ELECTROPHORETIC COMPARISON OF ENZYMES OF BALLISTOSPOROGENOUS YEASTS MASASHI YAMAZAKI AND KAZUO KOMAGATA The Institute of Applied Microbiology, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan (Received February 1, 1983) The patterns produced by nine enzymes of ballistosporogenous yeasts and supposedly related yeasts were studied by electrophoresis on poly- acrylamide gel. Forty-two strains belonged to the genera Sporobolomyces, Sporidiobolus, Aessosporon and Bullera and twenty-four strains to Rhodo- torula, Rhodosporidium, Cryptococcus, unidentified ballistosporogenous yeasts, and Candida edax. Four Sporobolomyces salmonicolor strains, two Sporobolomyces holsaticus strains, two Sporobolomyces odorus strains, five Sporidiobolus salmoni- color strains, two Aessosporon salmonicolor strains, and one strain of Aessosporon dendrophilum produced similar electrophoretic patterns. Moreover, mating was observed between some of these strains. Sporo- bolomyces roseus and Sporobolomyces shibatanus differed from Sporobolo- myces salmonicolor in their glucose-6-phosphate dehydrogenase (EC 1.1.1.49.), but the patterns of the other enzymes were similar; all three species differed clearly from Sporobolomyces singularis, Sporobolomyces gracilis, Sporobolomyces puniceus, and Sporobolomyces antarcticus. Sporobolomyces albo-rubescens showed a peculiar 6-phosphogluconate dehydrogenase (EC 1.1.1.41.) pattern and was similar to two Rhodotorula rubra strains in the pattern of their enzymes. Close relationships were also seen between Sporidiobolus ruinenii and Rhodotorula graminis, and between Bullera alba and a strain in Cryptococcus albidus var. albidus in the electrophoretic patterns of their enzymes. Four unidentified strains which had lost the ability to produce ballistospores had patterns similar to those of Bullera alba, Rhodotorula glutinis, Cryptococcus laurentii var. flavescens, and Cryptococcus macerans. Three colorless strains, putatively derived from a strain of Sporobolomyces roseus, showed the same electrophoretic patterns as the strains from which they originated. Ballistosporogenous yeasts differ from other yeasts in producing ballistospores Address reprint requests to: Dr. M. Yamazaki, The Institute of Enology and Viticulture, Yamanashi University, 13-1, Kitashin, 1-chome, Kofu 400, Japan. 115 116 YAMAZAKI and KOMAGATA VOL. 29 that are discharged at maturity by a drop-excretion mechanism. Three genera are described in "The Yeasts" (1): Bullera, Sporobolomyces, and Sporidiobolus. In 1970, VANDER WALT(2) found a homothallic sexual cycle in Sporobolomyces salmonicolor and proposed a new genus Aessosporon for it. FELLand TALLMAN(3) reported matings between strains of Aessosporon salmonicolor and some Sporo- bolomyces species. Thereafter, the sexual species Sporidiobolus salmonicolor and Sporidiobolus pararoseus were described as heterothallic species in the genus Sporidiobolus by FELL and TALLMAN(4). A close relationship between ballistosporogenous yeasts and some species of the genera Rhodotorula and Cryptococcus has been suggested by various biochemi- cal studies (5-14). In previous papers the present authors reported that electro- phoretic comparison of enzymes was a useful tool to clarify taxonomical relation- ships among strains of the genera Rhodotorula and Rhodosporidium (15), among strains of the genus Cryptococcus and related microorganisms (16), and between asporogenous yeasts and their supposed ascosporogenous states (17). The present paper deals with the electrophoretic comparison of nine enzymes of the genera Sporobolomyces, Sporidiobolus, Aessosporon, and Bullera, and discuss- es the relationship between ballistosporogenous yeasts and some strains of species of Rhodotorula, Rhodosporidium, and Cryptococcus. MATERIALSAND METHODS Yeast strains. The strains used and their sources are listed in Table 1. The identities of all of them were confirmed by the methods of "The Yeasts" (1) and BARNETTet al. (18). Cultivating and harvesting cells, preparation of cellfree extracts, and gel-slab electrophoresis. Methods for cultivating and harvesting cells, preparing cell-free extracts, and gel-slab electrophoresis were essentially the same as those reported previously (15). Staining procedures. The enzymes studied were fructose-l,6-bisphosphate aldolase (FA; EC 4.1.2.13.), 6-phosphogluconate dehydrogenase (6PGDH; EC 1.1.1.41.), malate dehydrogenase (MDH; EC 1.1.1.37.), glucose-6-phosphate dehydrogenase (G6PDH; EC 1.1.1.49.), glutamate dehydrogenase (GDH; EC 1.4.1.4.), hexokinase (HK; EC 2.7.1.1.), fumarase (Fina; EC 4.2.1.2.), phospho- glucomutase (PGM; EC 2.7.5.1.), and catalase (Cat; EC 1.11.1.6.). The staining procedures used for catalase were described by GREGORYand FRIDOVIcH(19) and for the other enzymes by SIcILIANOand SHAW(20). Figure 1 shows an example of a slab of polyacrylamide gel stained for seven enzymes of some ballistosporo- genous yeasts. The relative mobilities (Rm) of the enzyme bands were calculated as the ratio of the distance that the enzyme moved from the origin to the distance that the tracking dye (Bromophenol Blue) moved. Mating tests. Mating tests were made by mixing a loopful of cells of each of a 1983 Enzymatic Patterns of Ballistosporogenous Yeasts 117 Fig. 1. Polyacrylamide gel stained for FA, 6PGDH, GDH, MDH, Fina, HK, and PGM. Lane 1 and 2 (FA): 1, Sporidiobolus ruinenii YK 456; 2, Sporobolomyces albo- rubescens YK 421. Lane 3-5 (6PGDH): 3, Sporidiobolus johnsonii YK 457; 4, Spori- diobolus salmonicolor YK 400; 5, Sporidiobolus pararoseus YK 415. Lane 6-8 (GDH) : 6, Bullera alba YK 460; 7, B, alba YK 461; 8, Sporobolomyces albo-rubescens YK 422. Lane 9-11(MDH) : 9, Bullera alba YK 461;10, B. piricola YK 464;11, B, tsugae YK 465. Lane 12-18 (Fma) :12, Sporobolomyces roseus YK 418;13, S. roseus YK 419;14, S. roseus YK 420; 15, S, odorus YK 410; 16, S. odorus YK 411; 17, Sporidiobolus salmonicolor YK 412;18, Sporobolomyces odorus YK 413. Lane 19-21(HK): 19, Sporobolomyces sal- monicolor YK 403; 20, Aessosporon salmonicolor YK 451; 21, Sporidiobolus salmonicolor YK 407. Lane 22-25 (PGM) : 22, Bullera alba YK 460; 23, B. alba YK 461; 24, B. alba YK 462; 25, Unidentified YK 482. given pair on corn-meal agar plates. The plates were incubated for 1-2 weeks at 18°, and the growth of the mixed cells was inspected at intervals with the naked eye and microscopically. Teliospore germination followed the standard method (1). RESULTS Assimilation patterns of carbon compounds and potassium nitrate by strains used Table 2 shows the assimilation of thirty-two carbon compounds and potas- sium nitrate by the main ballistosporogenous yeasts and the putatively related yeasts. The assimilation patterns of these strains tested agreed well with those given in "The Yeasts" (1) and BARNETTet al. (18). Two strains, YK 416 and YK 417, are identified as Sporobolomyces pararoseus by the system of "The Yeasts" (1), but we called them Sporobolomyces shibatanus because FELL and TALLMAN(4) have changed the name. Four unidentified strains, YK 481, YK 482, YK 484, and YK 485, had lost the ability to produce ballistospores during preservation. The assimilation pattern of strain YK 481 was closest to that of Sporobolomyces roseus and Rhodotorula glutinis. Two strains, YK 482 and YK 484, closely resembled 118 YAMAZAKI and KOMAGATA VOL. 29 1983 Enzymatic Patterns of Ballistosporogenous Yeasts 119 120 YAMAZAKI and KOMAGATA VOL. 29 Table 2. Assimilation of carbon compounds and potassium nitrate Bullera alba and Cryptococcus laurentii in their assimilation patterns. The strain YK 485 and Cryptococcus macerans had similar assimilation patterns. Three colorless strains, YK 486, YK 487, and YK 488, showed the same assimilation patterns as Sporobolomyces roseus. Electrophoretic comparison of enzymes in the genus Sporobolomyces The relative electrophoretic mobilities (Rm) of nine enzymes from twenty- three strains of eleven Sporobolomyces species and one strain of Candida edax are 1983 Enzymatic Patterns of Ballistosporogenous Yeasts 121 shown in Table 3. Sporobolomyces holsaticus YK 401 and YK 402 produced identical patterns for nine enzymes. Sporobolomyces salmonicolor YK 403, YK 404, YK 405, and YK 406 exhibited identical patterns in FA, 6PGDH, Fina, HK, and GDH . There were two types of G6PDH : one was detected at Rm 0.23 (YK 403 and YK 404), the other at Rm 0.20 (YK 405 and YK 406). The patterns of MDH and Cat show- ed slight variations among the four strains. In addition , the PGM of YK 404 differed from the other three strains. The four Sporobolomyces odorus strains 122 YAMAZAKI and KOMAGATA VOL. 29 tested split into two pairs in their electrophoretic patterns. The first pair (YK 410 and YK 411) differed from the second (YK 413 and YK 414) in their 6PGDH, Fina, MDH, HK, PGM, GDH, and Cat patterns. No FA activity was detected in the second pair. Of the three Sporobolomyces roseus strains tested, YK 419 and YK 420 produced identical patterns for all nine enzymes. The other strain YK 418 resembled them with respect to its 6PGDH, Fma, G6PDH, and GDH pattern but not MDH, HK, PGM, and Cat. Sporobolomyces shibatanus YK 416 and YK 417 were identical in the 6PGDH, Fma, MDH (Rm 0.33), G6PDH, HK, GDH, and Cat enzymes but not in PGM ; no FA activity was detected in either of them. Sporobolomyces albo-rubescens YK 421 and YK 422 had identical patterns 1983 Enzymatic Patterns of Ballistosporogenous Yeasts 123 for all nine enzymes. They had a 6PGDH with three bands, at Rm 0.38, 0.40, and 0.42. Sporobolomyces
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