Yeast Research: A Historical Overview
Editors: James A. Barnett1, Linda BarnettCategory: Fungi and Fungal Pathogenesis; History of Science
Yeast Research, which was originally concerned with improving wine-making and brewing processes, has played a major role in the development of a number of modern scientific disciplines. In the 20th century, investigations of yeasts laid the foundations for mitochondrial genetics and cell cycle research. Today, thousands of people are engaged in research on yeasts, studying their physiology, metabolism, genetics, and molecular biology and developing new applications for industry and medicine. The book describes the historical background of this important work.
This book reviews the history of yeast research, beginning with fermentation research at the end of the 18th century. It traces our growing understanding of yeasts and their role in the evolution of microbiology, biochemistry, cytology, and genetics, and it includes an account of research on medical yeasts. Readers will learn how findings in yeast research were used to overcome complex problems and to develop currently accepted scientific concepts and methods.
Author James Barnett has worked on yeasts in the laboratory for 50 years and accordingly emphasizes experimental evidence, reproducing many figures from the original researchers’ work as well as illustrations of the equipment they used. The book is enlivened with images of many of the scientists and offers accounts of notable incidents in the lives of some of them.
More than 2,400 references are included, and there are many direct quotations from these sources. With its detailed discussions of the development of theory, methods, and techniques, Yeast Research: a Historical Overview serves as a key resource for anyone teaching or learning microbiology, biochemistry, or general biology.
Hardcover, 379 pages, illustrations, indexes.
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Chapter 1 : The Cause of Fermentation: Work by Chemists and Biologists, 1789 to 1850
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This chapter describes (i) the first major chemical analyses of ethanolic (wine) fermentation, (ii) the conclusive demonstration in the early 19th century that yeasts are microbes and cause the fermentation of beer and wine, and (iii) a remarkable attack on these microbiological findings by some of the most influential scientists of the time. Indeed, the first scientific research on yeast was done not by biologists but almost exclusively by chemists, who were investigating alcoholic fermentation. One of these—the great French chemist Antoine Lavoisier— described the phenomenon of alcoholic fermentation as "one of the most extraordinary in chemistry." In order to investigate, during fermentation, the conversion of sugar into carbon dioxide and alcohol, Lavoisier carried out a number of analyses, estimating the proportions of the chemical elements in sugar, water, and yeast paste. Schwann held that yeast cells caused fermentation, because fermentation was constantly associated with yeast propagation and failed when the yeast was destroyed by heat. He also commented that the yeast itself also increased in quantity during fermentation as Jean Jacques Colin had already observed and that this kind of phenomenon was displayed only by living organisms. In 1839, Jöns Jacob Berzelius stated that evidence from microscopy was of no value and that yeast was no more an organism than was precipitate of alumina; he also claimed that fermentation occurred by means of catalysis.
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Chapter 2 : The Beginnings of Yeast Physiology, 1850 to 1880
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We know that an analogous decomposition of salicin is produced by emulsin; neither in the one case nor in the other, is it possible to detect a physiological act. But between 1855 and 1875 Pasteur established unequivocally (i) the role of yeast in alcoholic fermentation, (ii) fermentation as a physiological phenomenon, and (iii) differences between the aerobic and anaerobic utilization of sugar by yeasts. The first part of Pasteur's paper deals with the changes in sugar which are brought about by alcoholic fermentation. The second part considers especially the "ferment", its nature, and the transformations it undergo. Pasteur's work on beer and wine yeasts gives some account of different yeasts, although he was never much interested in taxonomy. Indeed, his work Études sur la Bière described some elegant experiments on yeasts associated with wine grapes, probably carried out in the autumn of 1872. In 1862 Pasteur had discussed the sources of wine yeasts, describing how yeasts could be found in different fruit juices of high acidity, although if the juices were less acidic, bacteria would grow too. By 1880, alcoholic fermentation as a sign of the physiological activity of yeasts was not quite yet scientific orthodoxy. Up to that time, the finding of independent enzymic activity, separated from that of living cells, impeded understanding of the role of enzymes in cellular activity.
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Chapter 3 : Pure Cultures, New Yeast Species, and Cell-Free Extracts, 1880 to 1900
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This chapter concentrates on the years 1880 to 1900, when pure yeast cultures were first obtained, many new species were described, cell-free yeast extracts that could ferment sugars were made, and much was learned about sugar metabolism by yeasts. Some species were discovered by examining the traditional fermented drinks of various countries. Pasteur’s method of cultivating yeasts had not given pure cultures, since he transferred a small portion of a culture by means of a sterile instrument to sterile liquid medium and, when fresh growth occurred, he used this new growth to again inoculate sterile medium. The development of techniques for producing pure cultures also made the reliable descriptions of new species practicable, and about 130 kinds of yeast were reported or described between 1880 and 1900. To be consistent, perhaps yeast taxonomists should reattribute certain species, such as some species of the genus Tremella, as they too were described before the use of pure cultures became practicable. As well as beer and wine, other traditional fermented drinks examined microbiologically included ginger beer from England, sake from Japan, and kefir from the Caucasus. A markedly different method of obtaining active cell-free extracts of yeasts was developed by Henry Dixon and William Atkins at Trinity College Dublin: they extracted “zymase” from a Guinness brewery yeast by freezing it in liquid air.
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Chapter 4 : Yeast Cytology, 1890 to 1950
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This chapter gives a coherent account of the gradual and uneven emergence of understanding of yeast cytology. Indeed, although the vacuole is usually the largest organelle in a yeast cell, Guilliermond was absolutely right: for many years, the identities of the yeast vacuole and nucleus were confused by a number of authors. The vacuole, it is now known, is bounded by a single membrane, the tonoplast, and acts as a lysosome, particularly for nonspecific intracellular proteolysis. The ascospores (the products of meiotic cell division) had long been known to exist in certain yeasts and other fungi, but their sexual significance was not understood. In 1891, Hansen published a paper on ascospore germination in S. cerevisiae, Saccharomycodes ludwigii, and Pichia anomala. Certain specialized yeast cells, ballistoconidia and chlamydospores, were clearly described at the end of the 19th century, but studies on yeast dimorphism have been done mostly in the 20th century. Since 1950, the existence and characteristics of most organelles of yeasts, such as mitochondria, Golgi apparatus, and endoplasmic reticulum, have been established largely by the use of phase-contrast and electron microscopy, as well by advances in biochemistry, genetics, and molecular biology.
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Chapter 5 : Yeast Cytology, 1950 to 1990
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This chapter summarizes selected and somewhat disparate advances made in yeast cytology after about 1950. Northcote and Horne disintegrated their baker’s yeast mechanically, and after centrifuging, mounted the cell wall fraction in polyvinyl formal films. The yeast walls proved to be stratified: after acid hydrolysis, chromatography showed that the outer layer was mainly mannan-protein; the walls contained 29% glucan and 31% mannan, previously reported for yeast cell walls as 13% protein and 8.5% lipid . It was in 1956 that Necas described the formation of some protoplasts or spheroplasts amongst spontaneously autolyzing S. cerevisiae. In 1989, Hartwell emphasized the relevance of this work on the cell cycle for the prevention of mammalian cancers. Chromosome behaviour in meiosis is well characterized from cytological and genetic descriptions but little is known of the underlying molecular mechanisms, largely because no one experimental system has been developed to support an integrated application of modern cytological, genetic, and molecular biological methods. A thorough account of the amount of work published on yeast cytology in the last 50 or so years would occupy several volumes; in addition, no account has been given here of advances made since 1990, which involve such innovations as the green fluorescent protein reporter system, confocal microscopy, and flow cytometric analysis.
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Chapter 6 : The Fermentation Pathway, 1900 to 1950
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This chapter on fermentation pathway during the period 1900 to 1950, records how the metabolic pathway of alcoholic fermentation was gradually revealed during the first half of the 20th century and provides chronological summary of the metabolic pathway. During the first half of the 20th century, the role of phosphates in glycolysis was studied extensively and the course and nature of alcoholic fermentation by yeasts and of lactic acid production by muscles were thus uncovered. This research provided the key to understand other metabolic processes, including the energy-transforming machinery of living cells. The first account of the formation of ATP, produced at the expense of energy derived from glycolysis, was published in 1934 when Jacob Karol Parnas, Pawel Ostern, and Thaddeus Mann reported the transfer of phosphate from phosphoglycerate to the adenylic acid system in muscle and Karl Lohmann and Otto Fritz Meyerhof discovered phosphoenolpyruvate. Although this chapter names only some of the many research workers and lists merely a few of the relevant publications, it summarizes the enormous amount of research on glycolysis carried out in the first half of the 20th century. The intricate and labyrinthine story of elucidating the fermentation pathway is complicated by the involvement of two systems, alcoholic fermentation by yeasts and lactic acid fermentation by muscles.
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Chapter 7 : The Main Respiratory Pathway, 1920 to 1960
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This chapter on main respiratory pathway covers the history of research on both the tricarboxylic acid (TCA) cycle and the cytochrome system. The first account of the TCA cycle came after the elucidation of the part played by cytochromes in respiration, but the account of the research on the cytochromes is here given second because, in terms of physiology, the activity of the cytochromes depends on the TCA cycle. The concept of free energy produced by intracellular oxidations depended on the early findings in thermodynamics, and in the second half of the same century, Moritz Traube did much to develop the idea of intracellular oxidations in relation to respiration and fermentation. Establishing the TCA cycle as the main pathway of carbohydrate oxidation in yeasts had to wait another 20 years. The impermeable nature of the plasma membrane and the lack, in Saccharomyces cerevisiae, of carriers which take succinate and other intermediates of the cycle into the cytosol, were the chief obstacles for realizing that the TCA cycle operates in yeasts, just as it does in plants and animals.
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Chapter 8 : Enzymic Adaptation and Regulation, 1900 to 1960
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Most of the work which explained the general phenomenon of enzymic adaptation was done by studying the microbial utilization of lactose and d-galactose, both of which have long been relatively easy to obtain and purify. This chapter concentrates on the utilization of these two sugars. Three different lines of research have provided the basis for understanding adaptations by yeasts and other microbes. The first was the work on galactose utilization by yeasts, published by Frédéric Dienert in 1899 and 1900. Second, the remarkable adaptive pathway of d-galactose catabolism by yeasts was worked out by Luis Leloir and his colleagues between 1948 and 1952. Finally, in the 1950s and 1960s, Jacques Monod, François Jacob, André Lwoff , and their confrères explained microbial adaptations largely in terms of induction and repression of enzyme synthesis, regulated by a complex of genes. By the late 1940s, the fermentation of galactose by yeasts had become the most thoroughly studied system of enzymic adaptation. Georges Cohen and Monod argued that the entry of organic substrates into microbial cells is mediated by more or less selective permeation systems, which they proceeded to characterize. During the 1950s, Monod and his colleagues isolated many mutants from Escherichia coli. In 1956, their seminal findings were published, which led them to the concept of "permeases". The genetic regulatory mechanism of Saccharomyces cerevisiae, acting on the GAL genes which encode the enzymes of galactose utilization, has been the most intensively studied and has become the best-understood genetical regulatory mechanism in any eukaryote.
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Chapter 9 : Regulation of Sugar Metabolism, 1920 to 2004
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This chapter includes an account of the investigation of certain well-known, general regulatory mechanisms that control sugar metabolism, which involves enzyme induction, repression, and inactivation. Some of the mechanisms which regulate sugar metabolism have been named after those who first described the respective phenomena: the Pasteur, Kluyver, Custers, and Crabtree effects. Other general regulatory phenomena are glucose or catabolite repression and glucose or catabolite inactivation. However, what has been called the Crabtree effect in yeasts should be called ‘’glucose repression’’. All these effects involve regulatory changes in the amounts of enzyme synthesis or of enzyme activity, or both. The author along with Tony Sims extended the notion of the Kluyver effect to the utilization of D-galactose. The chapter provides the basis for understanding the roles of the Snf kinase and Mig1p in glucose repression through a series of observations. The Pasteur, Kluyver, and Custers effects are responses by yeasts to changes in the amount or character of the sugars available to them. Enzymic regulation, induction, repression, and inactivation bring about these effects and make possible other adaptations to alterations in the supplies of nutrients. The first major analysis of a microbial adaptation, carried out during the 1960s to 1980s, was that of the induction and repression of enzymes of the galactose pathway in Saccharomyces cerevisiae. Research on the molecular biology of cellular regulation is very active today and will undoubtedly bring to light even greater complexities.
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Chapter 10 : Metabolite Transport by Facilitated Diffusion, 1900 to 2000
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This chapter on metabolite transport by facilitated diffusion describes some of the history of studying how molecules move across cell membranes, particularly yeast membranes. In discussing how substances both enter and leave yeast cells, it is necessary to consider the structures through which the substances must pass, namely, the cell wall and the plasma membrane, as well as intracellular membranes. Steveninck and Rothstein suggested that while uptake involves sugar phosphorylation, when glycolysis is prevented by iodoacetate, sugar uptake occurs by facilitated diffusion. The results of pulse-labeling experiments indicated that uptake of galactose by baker’s yeast was adaptive and probably involved entry of the free sugar and its accumulation to diffusion equilibrium. The following three independent findings were consistent with this conclusion. First, the high-affinity mode of galactose uptake was found to depend on the presence of galactokinase. Second, from pulse-labeling studies of glucose uptake by a wild-type yeast, via a carrier of low Km, Kotyk published convincing evidence that free sugar in the intracellular pool was labeled first. Finally, the route with a high Km, in a kinaseless yeast strain, conformed to the established pattern of a facilitated diffusion pathway. The results suggest that high-affinity glucose transport is not necessarily dependent on the presence of glucose-phosphorylating enzymes. Apparent low-affinity uptake kinetics can arise as a consequence of an insufficient rate of removal of intracellular free glucose by phosphorylation.
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Chapter 11 : Metabolite Uptake by Active Transport, 1925 to 2000
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This chapter deals with the kind of transport which is activated by metabolic energy, with solutes crossing membranes against their own gradient of electrochemical potential. In the 1940-50s, evidence of active transport of ions, amino acids, and glycosides was also reported for bacteria and for human erythrocytes. 2,4-dinitrophenol (DNP) inhibits active transport as it uncouples oxidative phosphorylation, mediating proton conductance across the inner membrane of the mitochondria. By the mid-1970s, proton symport was established as a means by which some substrates enter certain bacteria. Indeed, the concentration of certain amino acids and sugars by various mammalian and bacterial cells had been shown to depend on the coupling of transport to the flow of specifications, such as Na+, K+, or H+. Although most of the research on metabolite transport into yeasts has been done with saccharomyces cerevisiae, there has been a good deal of work on transport into several other species, especially during the 1970-80s. A glucose-repressible carrier was described in 1975 for K. lactis as taking up succinate, L-malate, fumarate, and 2-oxoglutarate by active transport. The occurrence of active transport of solutes into cells, with the energy being supplied by metabolism, was established in the 1930s by work on plant roots. At about the same time, the concentration of solutes by animal cells was also observed. However, biochemists generally failed to think of transport as a metabolic activity until Jacques Monod and his colleagues laid the foundations of membrane transport as an important part of metabolic studies in the 1950s.
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Chapter 12 : The Foundations of Yeast Genetics, 1918 to 2000
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This chapter provides an account of some of the early works on yeasts which laid the foundations for several major developments in genetics as a whole. Much of the pioneer and totally academic work on yeast genetics was done at the Carlsberg Laboratory in Copenhagen between 1935 and 1955, largely by the Danish geneticist Øjvind Winge, who can reasonably be regarded as the founder of yeast genetics. In 1939, Winge and Laustsen confirmed Guilliermond’s earlier suggestion that Saccharomycodes ludwigii is heterothallic. Working with Neurosporacrassa, in 1933, Lindegren had suggested that the frequency of crossing-over between a gene and its centromere was a measure of their distance apart on the linkage map. It should be mentioned here that in 1985, electrophoretic karyotyping showed that Saccharomyces cerevisiae has a haploid number of 16 chromosomes, and this was confirmed later. In the absence of sexual reproduction, genetic mapping begun in the early 1980s, by fusing spheroplasts, so that recombination analyses became practicable. Work on the cell cycle in S. cerevisiae and Schiz. pombe has enormously increased the understanding of how cell growth is controlled and, hence, has provided information which will assist in developing the medical control of human cancers. The genetic tractability of S. cerevisiae and its nonpathogenic character have made it attractive for elucidating cellular biochemistry and facilitating the molecular analysis of genes which cause diseases. It is used for testing antifungal products and other new drugs.
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Chapter 13 : Medical Yeasts, 1800 to 2000
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This chapter mainly focuses on the two major pathogenic yeast species, namely, Candida albicans, the most widespread yeast pathogen, and Cryptococcus neoformans, which is probably the most lethal of the yeast pathogens. The study of chlamydospores goes back a long way, with Grawitz describing in 1877 how these cells in C. albicans develop from hyphae, germinate, and give rise to more hyphae. Cells enveloped by capsules of polysaccharide have long been known to be characteristic of yeasts of the genus Cryptococcus and thought to be important for the virulence of Cr. neoformans in addition to its ability to grow at 37°C, which is crucial for its pathogenicity; other Cryptococcus species do not grow at that temperature. Serologically active polysaccharides from microbes had been known ever since 1927, when Dorothea Smith described the capsular substance of Escherichia coli. In this paper she showed that there is a close association between the production of specific polysaccharides, the capsular material, and the virulence of the bacterium. The scientific interest in pathogens is likely to lie primarily in their detailed differences from similar organisms which are not pathogenic. This circumscription has been offset to some extent by the greater ease with which financial support has been available for work on pathogens rather than purely academic research.
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Chapter 14 : Yeast Taxonomy, 1900 to 2000
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As well as isolating new species, taxonomists have, almost uniquely undertaken the comparative study and description of many different kinds of yeast, and this is probably one of their most valuable contributions to yeast biology. This chapter considers some aspects of the history of all these kinds of activity. Ascospore-forming yeasts, such as Saccharomyces species, were isolated notably from industrial fermentations, whereas many non-ascospore-producing yeasts were found in clinical practice-for example, Candida albicans and Malassezia furfur, often the putative causes of mycotic diseases. In 1924, Endomyces fibuliger was transferred to Saccharomycopsis. However, the genus Saccharomycopsis generally lapsed into desuetude until Kreger-van Rij restored it in all its glory in 1984. Writing from the Faculté de Médecine of Paris in 1932, Maurice Langeron and Rodolfo Talice published a paper on classifying those fungi which characteristically formed both filaments and yeast-like cells. This paper was largely a report of a microscopical study of the different categories of cell produced by each kind of yeast: blastoconidia, chlamydospores, the mode of budding, and the greatly varied appearance of filamentous growths. The chapter describes the inception of some genera which were thought to be asexual, namely, Brettanomyces, Sporobolomyces, Bullera, Rhodotorula, Kloeckera, Trigonopsis, and Schizoblastosporion. The sensible naming of yeasts is vital for all who work with them, in research, in commerce, and in medicine.
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Microbiology Today
16 July 2013
This unique book has been developed from a number of articles originally published in Yeast. Written by a scientist for scientists, it covers research from the late 18th century until the year 2000. There are many useful figures, interesting original quotations (including from those who got things completely wrong) and entertaining photographs of some of the key protagonists. It is a book to dip into, and I always found myself hooked and read more than I planned to. Yeasts are now at the forefront of genetics research, but this book reminds us of their seminal importance in the development of biochemistry and microbiology amongst other sciences. Putting research into the historical context of how we got where we are today, it should be in the library of all institutions where these sciences are studied. Students should be encouraged to read parts of it even if only to show them that there was science before genomics!
Society for General Microbiology: Microbiology Today
Reviewer: Alan Wheals, University of Bath
Review Date: August 2012