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Chemical and Cytological Changes During CHEMICAL AND CYTOLOGICAL CHANGES DURING THE AUTOLYSIS OF YEASTS A thesis submitted to The University of New South Wales as fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY by Tatang Hernawan Sarjana Farmasi, Apoteker (I T B, Indonesia) Master of Applied Science (UN SW, Australia) Department of Food Science and Technology The University of New South Wales Kensington, N. S. W. Australia February 1992 D E C L A R A T I O N The candidate, Tatang Hernawan, hereby declares that this thesis is his own work and that, to the best of his knowledge and belief, it contains no material previously published or written by another person nor material which to substantial extent has been accepted for the award of any degree or diploma of a university or other institute of higher learning, except where due acknowledgement is made in the text of the thesis. T a t a n g H e r n a w a n A C K N O W L E D G E M E N T S I wish to express my sincere gratitude to Associate Professor G. H. Fleet, Department of Food Science and Technology, University of New South Wales, Australia, as my supervisor for his guidance, advice and encouragement during this project and thesis production. I would like to acknowledge the assistance of laboratory staff of the Department of Food Science and Technology, Mr P. Mark, of the Electron Microscopy Unit, and Ir E. Poerwanto, a fellow postgraduate student, University of New South Wales. I would like to thank fell ow students in the Department of Food Science and Technology for a friendly situation throughout this study and Ms H. N. Ivan for helping me during studies in Australia. Sincere thanks are also given to my father, Mr H. Sadeli, during his life, and my mother, Mrs H. Oyoh Sadeli for their strong encouragement and support. To my children, Rogydesa and Bethasari, and my wife, Ora Ny. Nila Merli ta, I would like to thank them for their support during this study. I would like to thank the Commonwealth Government of Australia for granting me a Colombo Plan Award, and the Department of Food Science and Technology, University of New South Wales, and the Department of iii Pharmacy, Bandung Institute of Technology, Indonesia, for facilitating my PhD studies. iv T A B L E 0 F C O N T E N T S Page ACKNOWLEDGEMENTS . iii TABLE OF CONTENTS . v ABSTRACT . ix 1. INTRODUCTION . 1 2. LITERATURE SURVEY . 6 2.1 Autolysis - General Description ............ 6 2.2 Subcellular Organisation Of Yeast .......... 7 2.2.1 Cell wall............................ 7 2.2.2 Cytoplasmic membrane .............. ... 11 2. 2. 3 Organelles . 12 2.3 Cytological Changes During Autolysis Of Yeast 16 2.4. Biochemical Changes During Autolysis ...... 19 2.4.1 Carbohydrates ........................ 19 2.4.2 Proteins ............................. 22 2. 4. J Nucleic acids . 34 2.4.4 Lipids ............................... 38 2.4.5 Vitamins ............................. 50 2.5 Commercial Significance Of Yeast Autolysis . 51 2.5.1 Leavening power of compressed baker's yeast ................................ 52 2.5.2 Autolysed yeast extracts 52 2.5.J Industrial fermentations 53 3. MATERIALS AND METHODS ...... ... ...... ......... .. 57 3 .1 Yeast Strains And Culture . 57 3. 2 Autolysis Of Yeast Cells . 59 V 3.3 Cell Viability . 59 3.4 Cell Dry Weight; Soluble Autolysate ....... 59 3.5 Total Carbohydrate, Reducing Sugar. And Glucose. 60 3. 6 Organic Acids . 61 3.7 Protein 62 3.8 Amino Acids 62 3.9 Ribonucleic Acid 64 3.10 Deoxyribonucleic Acid ..................... 66 3.11 Lipids . 68 3.12 Free Fatty Acids . 70 3 .13 Glycerol . 71 3.14 Cytological Observations .................. 72 4. RESULTS . 75 4.1 Comparative Survey Of Autolysis In Several Species And Strains Of Yeasts . 7 5 4.1.1 Introduction ......................... 75 4.1.2 Results .............................. 75 Cell viability 75 Solubilization of cell biomass ........ 76 Reproducibility of data on dry weight analysis .............................. 78 Carbohydrates 78 Organic acids 78 Protein 84 Amino Acids 84 Ribonucleic acid 88 Deoxyribonucleic acid . 92 Lipid 94 vi Free Fatty Acids . 104 4.2 Chemical Changes During The Autolysis Of Saccharomyces cerevisiae 2180a, Kloeckera apiculata 202 And Candida stellata 8008 ..... 104 4.2.2 Introduction ......................... 104 4.2.3 Results ............................... 104 Cell viability 104 Solubilization of cell biomass ......... 106 Carbohydrates 106 Organic acids 111 Protein 114 Amino acids 114 Ribonucleic acid (RNA) 119 Deoxyribonucleic acid (DNA) 119 Lipids . 124 Glycerol . 130 4.3 Effect Of Cell Concentration On The Kinetics Of Yeast Autolysis . 130 4.3.1 Introduction 130 4.3.2 Results .............................. 134 Effect of cell concentration on the kinetics of cell death during autolysis. 134 Effect of cell concentration on the kinetics of cell weight changes and cell solubilization during autolysis ........ 134 4.4 Observations Of Yeast Autolysis With The Electron Microscope ........................ 136 4. 4 .1 Introduction . 136 4.4.2 Results .............................. 139 Scanning electron micrographs of auto- lysing yeasts . 139 Transmission electron micrographs of thin sections of autolvsing yeasts ..... 139 5. D I S C U S S I O N . 149 vii 5.1 Cell viability 150 5.2 Solubilization of cell biomass ............. 152 5.3 Carbohydrates 154 5.4 Organic acids 156 5.5 Proteins and Amino Acids ................... 159 5. 6 Nucleic acids . 164 Ribonucleic acid 164 =D~e~o~x-y~r~i=b~o~n~u=c-=l=e=i~c---aaa~c~i____ d ................. 166 5.7 Lipids . 168 5.8 Cytological changes ........................ 173 6. CON CL US ION ............................. 176 B I B L I O G R A P H Y . .. .. .. .. .. 182 viii ABSTRACT The chemical and cytological changes that occurred during the autolysis of three yeasts, Saccharomyces cerevisiae, Kloeckera apiculata, and Candida stellata, were examined. The yeasts were grown in yeast extract glucose broth for 48 h, after which the cells were harvested and autolysed by incubating in 0.1 M phosphate buffer, pH 4.5, at 45"C for up to 10 days. Three strains of each species were examined. Autolysis was characterised by rapid loss in cell viability and solubilization of cell biomass. After 10 days, 25-35 % of the cell dry weight was solubilized. The soluble autolysate consisted of carbohydrate (3-7 %), organic acids (3-6 %), protein (12-13 %), free amino acids (8-12 %), nucleic acids (3-5 %) , and lipids (1-2 %) , Carbohydrate in autolysates was predominantly polysaccharide with only traces of glucose or reducing sugars. The main organic acids in autolysates were propionic, succinic, oxalic, acetic, formic, and malic, with some variation in their individual concentrations depending on yeast species. Sixteen different free amino acids were found in autolysates, the main ones being phenylalanine, glutamic acid, leucine, alanine, and arginine. The concentrations of individual amino acids varied with yeast strain. Cellular RNA was 85-90 % degraded during autolysis with most of the degradation products appearing in the autolysates. Cellular DNA was only partially degraded and recovered in the autolysates. Approximately 40 % of cell lipid was lost during autolysis and recovered in autolysates. Both phospholipid and neutral lipid classes were degraded, with neutral lipids but not phospholipids being found in autolysates. The composition of cellular lipids as well as degradation of the different lipid classes varied with the yeast species. Autolysates contained 0.2-0.6 % glycerol. Scanning electron microscope and transmission electron microscope observations showed the cell shape and cell wall to remain intact during autolysis, although a decrease (13-14 %) in wall thickness was noted. After 5 days of autolysis, there was a retraction of the cell membrane from the cell wall, and some mernbraneous vesicularization. Such cytological changes were less evident in K. apiculata. There were minor variations in autolytic behaviour between strains of one species. The autolytic character of K. apiculata showed significant differences from the other two species. X 1 1. INTRODUCTION Autolysis or self degradation is a natural event that occurs after yeast cells have completed their normal growth cycle and have entered tt.e death phase. In general terms, it is characterized by a loss of membraneous function and organization, degradation and solubilization of cell macromolecules by th~ action of endogenous enzymes and the release of intracellular constituents and br_eakdown products into the extracellular environment. The phenomenon of autolysis in baker's yeast was first observed by Salkowski at the end of the 19th century (see Farrer (1956) for historical review), and since that time it has attracted the sporadic interests of scientists. Of potential commercial interest, were the findings that yeast autolysates were rich in amino acids, proteins, vitamins, and ctegradation products of nucleic acids, and that the autolytic process could be significantly accelerated or triggered by incubating yeast cells at high temperature, by addition of salt, or by treatment with various organic solvents, such as, toluene, chloroform, or ethanoJ. The commercial implications of yeast autolysis are varied and have been recognized for a long time. Indeed, they have attracted more attention than endeavours to understand the scientific basis of the process. Yeast autolysates, which are rich in nutrients 2 and strong in flavour profile, quickly found application as ingLedients in the food processing industries (Peppler 1982, Dziezak 1987ab). Autolysis was also seen as a process for preparing proteins, polysaccharides and pigments from various yeasts for use in the food and feed industries. Several enzymes, such as invertase and ~- galactosidase, also used in food processing, were prepared from yeast autolysates (Peppler 1982). On the negative side, it was quickly realized that autolysis was the process that decreased the leavening power of baker's yeast (Saccharomyces cerevisiae) during storage and that uncontrolled autolysis of brewer's and wine yeasts would lead to of £-flavours and bacterial spoilage problems in beer and wines.
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