Abstract
We have studied the biogenesis and enzymic composition of microbodies in different yeasts during adaptation of cells to a new growth environment. After a shift of cells of Candida boidinii and Hansenula polymorpha from glucose to methanol/methylamine-containing media, newly synthesized alcohol oxidase and amine oxidase are imported in one and the same organelle together with catalase; as a consequence the cells contain one class of morphologically and enzymatically identical microbodies. Similar results were obtained when Candida utilis cells were transferred from glucose to ethanol/ethylamine-containing media upon which all cells formed microbodies containing amine oxidase and catalase.
However, when methanol-limited cells of H. polymorpha were transferred from media containing ammonium sulphate to those with methylamine as the nitrogen source, newly synthesized amine oxidase was incorporated only in part of the microbodies present in these cells. This uptake was confined to the few smaller organelles generally present at the perimeter of the cells, which were considered not fully developed (immature) as judged by their size. Essentially similar results were obtained when stationary phase cells of C. boidinii or C. utilis — grown on methanol and ethanol plus ammonium sulphate, respectively — were shifted to media containing (m)ethylamine as the nitrogen source. These results indicate that mature microbodies may exist in yeasts which no longer are involved in the uptake of matrix proteins. Therefore, these yeasts may display heterogeneities in their microbody population.
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References
Bellion E, Goodman JM (1987) Proton ionophores prevent assembly of a peroxisomal protein. Cell 48:165–173
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
Douma AC, Veenhuis M, Sulter GJ, Harder W (1987) A protontranslocating adenosine triphosphatase is associated with the peroxisomal membrane of yeasts. Arch Microbiol 147: 42–47
Frens G (1973) Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nature Phys Sci 241:20–22
Fukui S, Tanaka A (1979) Peroxisomes of alkane-and methanolgrown yeasts. Metabolic functions and practical applications. J Appl Biochem 1:171–201
Kitamura K, Kaneda T, Yamamoto Y (1971) Lysis of viable cells by enzymes of Arthrobacter luteus. Arch Biochem Biophys 145:402–404
Luck H (1963) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Acad Press New York London pp 885–894
Moor H (1964) Die Gefrier-Fixation lebender Zellen und ihre Anwendung in der Elektronenmikroskopie. Z Zellforsch 62:546–580
Nicolay K, Veenhuis M, Douma AC, Hader W (1987) A 31P NMR study of the internal pH of yeast peroxisomes. Arch Microbiol 147:37–41
Osumi M, Imaizumi F, Imai M, Sato H, Yamaguchi H (1975) Isolation and characterization of microbodies from Cancida tropicalis PK 233 cells grown on normal alkanes. J Gen Appl Microbiol 21:375–387
Slot JW, Geuze HJ (1984) Goldmarkers for single and double immunolabelling of ultrathin cryosections. In: Polak JM, Varndell IM (eds) Immunolabelling for electron microscopy. Elsevier Sci Publ. Amsterdam pp 129–142
Van Dijken JP, Veenhuis M, Vermeulen CA, Harder W (1975) Cytochemical localization of catalase activity in methanol-grown Hansenula polymorpha. Arch Microbiol 105:261–267
Van Dijken JP (1976) Oxidation of methanol by yeasts. Ph D Thesis University of Groningen, The Netherlands
Van Dijken JP, Otto R, Harder W (1976) 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
Veenhuis M, Harder W (1987) Metabolic significance and biogenesis of microbodies in yeasts. In: Fahimi HD, Sies H (eds) Peroxisomes in biology and medicine. Springer, Berlin Heidelberg New York, pp 435–457
Veenhuis M, Harder W (1988) Yeast microbodies. Their substructure, biogenesis and turnover in relation to environmental conditions. In: Rose AH (ed) The yeasts, vol 3. Academic Press, London (in press)
Veenhuis M, Van Dijken JP, Harder W (1976) Cytochemical studies on the localization of methanol oxidase and other oxidases in peroxisomes of methanol grown Hansenula polymorpha. Arch Microbiol 111:123–135
Veenhuis M, van Dijken JP, Pilon SAF, Harder W (1978) Development of crystalline peroxisomes in methanol-grown cells of the yeast Hansenula polymorpha and its relation to environmental conditions. Arch Microbiol 117:153–163
Veenhuis M, Keizer I, Harder W (1979) Characterization of peroxisomes in glucose grown Hansenula polymorpha and their development after the transfer of cells into methanol-containing media. Arch Microbiol 120:167–175
Veenhuis M, Zwart KB, Harder W (1981) Biogenesis and turnover of peroxisomes involved in the concurrent oxidation of methanol and methylamine in Hansenula polymorpha. Arch Microbiol 129:35–41
Veenhuis M, Van Dijken JP, Harder W (1983) The significance of peroxisomes in the metabolism of one carbon compounds in yeasts. Adv Microbiol Physiol 24:1–82
Veenhuis M, Hoogkamer-te Niet MC, Middelhoven WJ (1985) Biogenesis and metabolic significance of microbodies in urateutilizing yeasts Antonie van Leeuwenhoek J Microbiol Serol 51:31–38
Veenhuis M, van der Klei IJ, Harder W (1986) Physiological role of microbodies in the yeast Trichosporon cutaneum during growth on ethylamine as the source of energy, carbon and nitrogen. Arch Microbiol 145:39–50
Zagers J, Sjollema K, Veenhuis M (1986) Construction and use of an improved, inexpensive cabinet for low temperature embedding of biological tissue for electron microscopy. Laboratory Practice 35:114–115
Zwart K (1983) Metabolic significance of microbodies in the yeasts Candida utilis and Hansenula polymorpha. Ph D Thesis, University of Groningen, The Netherlands
Zwart K, Veenhuis M, Van Dijken JP, Harder W (1980) 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
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Veenhuis, M., Sulter, G., van der Klei, I. et al. Evidence for functional heterogeneity among microbodies in yeasts. Arch. Microbiol. 151, 105–110 (1989). https://doi.org/10.1007/BF00414422
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DOI: https://doi.org/10.1007/BF00414422