Abstract
The metabolism of methylamine as the nitrogen source for growth of the non-methylotrophic yeast Candida utilis and the methylotrophic yeast Hansenula polymorpha was investigated. Grwoth of both organisms in media with glucose and methylamine was associated with the presence of an amine oxidase in these cells. The enzyme catalyses the oxidation of methylamine by molecular oxygen into ammonia, formaldehyde and hydrogen peroxide and it is considered to be the key enzyme in methylamine metabolism in the organisms studied.
In addition to synthesis of amine oxidase, derepression of catalase, formaldehyde and formate dehydrogenase was also observed upon transfer of cells of the two organisms from media containing ammonium ions into media containing methylamine as the nitrogen source.
The synthesis of enzymes was paralleled by the development of a number of large microbodies in the cells. Cytochemical staining experiments indicated that the amine oxidase activity was located in the microbodies in both organisms. Catalase-activity was also demonstrated in these organelles, which can therefore be considered as peroxisomes. The present contribution is the first description of a peroxisomal amine oxidase.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Boadle, C. M., Bloom, F. E.: A method for the fine structural localization of monoamine oxidase. J. Histochem. Cytochem. 17, 331–340 (1968)
Brady, B. L.: Utilization of amino compounds by yeasts of the genus Saccharomyces. Antonie van Leeuwenhoek J. Microbiol. Serol. 31, 92–105 (1965)
Van Dijken, J. P., Veenhuis, M., Vermeulen, C. A., Harder, W.: Cytochemical localization of catalase activity in methanol-grown Hansenula polymorpha. Arch. Microbiol. 105, 261–267 (1975)
Van Dijken, J. P., Otto, R., Harder, W.: Growth of Hansenula polymorpha in a methanol-limited chemostat. Physiological responses due to the involvement of methanol oxidase as a key enzyme in methanol metabolism. Arch. Microbiol. 111, 137–144 (1976)
De Duve, C., Baudhuin, P.: Peroxisomes (microbodies and related particles). Physiol. Rev. 46, 323–326 (1966)
Eggeling, L., Sahm, H.: Derepression and partial insensitivity to carbon catabolite repression of the methanol dissimilatory enzymes in Hansenula polymorpha. Eur. J. Appl. Microbiol. Biotechnol. 5, 197–202 (1978)
Egli, Th., van Dijken, J. P., Veenhuis, M., Harder, W., Fiechter, A.: Methanol metabolism in yeasts: regulation of the synthesis of catabolic enzymes. Arch. Microbiol. 124, 115–121 (1980)
Feldman, J. M., Roche, J. M., Blum, J. J.: Monoamine oxidase and catechol-o-methyl transferase activity in Tetrahymena. J. Protozool. 24, 459–462 (1977)
Kitamura, K., Kaneda, T., Yamamoto, Y.: Lysis of viable cells by enzymes of Arthrobacter luteus. Arch. Biochem. Biophys. 145, 402–404 (1971)
Lang, E., Lang, H.: Spezifische Farbreaktion zum direkten Nachweis der Ameisensäure. Z. Anal. Chem. 260, 8–10 (1972)
Lloyd, D.: The mitochondria of microorganisms. London, New York, San Francisco: Acad. Press 1974
Moor, H.: Die Gefrief-Fixation lebender Zellen und ihre Anwendung in der Elektronenmikroskopie. Z. Zell.-Forsch. 62, 546–580 (1964)
Osumi, M., Imaizumi, F., Imai, M., Sato, H., Yamaguchi, H.: Isolation and characterization of microbodies from Candida tropicalis PK 233 cells grown on normal alkanes. J. Gen. Appl. Microbiol. 21, 375–387 (1975)
La Rue, T. A., Spencer, J. F. T.: Utilization of organic nitrogen compounds by yeasts of the genus Saccharomyces. Antonie van Leeuwenhoek J. Microbiol. Serol. 34, 153–158 (1968)
Roels, F., Wisse, E., de Prest, B., van der Meulen, J.: Cytochemical discrimination between catalases and peroxidases using diamino benzidine. Histochem. 41, 281–312 (1975)
Roon, R. J., Even, L. E., Dunlop, P.: Methylamine and ammonium transport in Saccharomyces cerevisiae. J. Bacteriol. 122, 502–509 (1975)
Sahm, H.: Metabolism of methanol by yeasts. Adv. Biochem. Engin. 6, 77–103 (1977)
Tani, Y., Kato, N., Yamada, H.: Utilization of methanol by yeast. Adv. Appl. Microbiol. 24, 165–186 (1978)
Veenhuis, M., van Dijken, J. P., Harder, W.: Cytochemical studies on the localization of methanol oxidase and other oxidases in peroxisomes of methanol-grown Hansenula polymorpha. Arch. Microbiol. 111, 123–135 (1976)
Veenhuis, M., Van Dijken, J. P., Pilon, S. A. F., Harder, W.: Development of crystalline peroxisomes in methanol-grown cells of the yeast Hansenula polymorpha and its relation to environmental conditions. Arch. Microbiol. 117, 153–163 (1978)
Veenhuis, M., Keizer, I., Harder, W.: Characterization of peroxisomes in glucose-grown Hansenula polymorpha and their development after the transfer to cells into methanol-containing media. Arch. Microbiol. 120, 167–175 (1979)
Van der Walt, J. P.: Utilization of ethylamine by yeasts. Antonie van Leeuwenhoek J. Microbiol. Serol. 28, 91–96 (1962)
Weibel, E. R., Bolender, P.: Stereological techniques for electron microscopic morphometry. In: Principles and techniques of electron microscopy (M. A. Hayat, ed.). London: Van Nostrand Reinhold 1976
Yamada, H., Adachi, O., Ogata, K.: Amine oxidases of microorganisms. Part II. Purification and crystallization of amine oxidase of Aspergillus niger. Agric. Biol. Chem. 29, 649–654 (1965b)
Yamada, H., Adachi, O., Ogata, K.: Amine oxidases of microorganisms. Part III. Properties of amine oxidase of Aspergillus niger. Agric. Biol. Chem. 29, 864–869 (1965c)
Yamada, H., Adachi, O., Ogata, K.: Amine oxidases of microorganisms. Part IV. Further properties of amine oxidase of Aspergillus niger. Agric. Biol. Chem. 29, 912–917 (1965d)
Yamada, H., Kumagai, H., Uwajima, T., Ogata, K.: Trimethylamine metabolism. I. Monomethylamine oxidase. Mem. Res. Inst. Food Sci. 27, 1–13 (1966)
Yamada, H., Kishimoto, N., Kumagai, H.: Metabolism of N-substituted amines by yeasts. J. Ferment. Technol. 54, 726–737 (1976)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Zwart, K., Veenhuis, M., van Dijken, J.P. et al. Development of amine oxidase-containing peroxisomes in yeasts during growth on glucose in the presence of methylamine as the sole source of nitrogen. Arch. Microbiol. 126, 117–126 (1980). https://doi.org/10.1007/BF00511216
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00511216