Fungi Read online

TAXATION Stephen Smith

  TEETH Peter S. Ungar

  TERRORISM Charles Townshend

  THEATRE Marvin Carlson

  THEOLOGY David F. Ford

  THOMAS AQUINAS Fergus Kerr

  THOUGHT Tim Bayne

  TIBETAN BUDDHISM Matthew T. Kapstein

  TOCQUEVILLE Harvey C. Mansfield

  TRAGEDY Adrian Poole

  THE TROJAN WAR Eric H. Cline

  TRUST Katherine Hawley

  THE TUDORS John Guy

  TWENTIETH‑CENTURY BRITAIN Kenneth O. Morgan

  THE UNITED NATIONS Jussi M. Hanhimäki

  THE U.S. CONGRESS Donald A. Ritchie

  THE U.S. SUPREME COURT Linda Greenhouse

  UTOPIANISM Lyman Tower Sargent

  THE VIKINGS Julian Richards

  VIRUSES Dorothy H. Crawford

  WATER John Finney

  WILLIAM SHAKESPEARE Stanley Wells

  WITCHCRAFT Malcolm Gaskill

  WITTGENSTEIN A. C. Grayling

  WORK Stephen Fineman

  WORLD MUSIC Philip Bohlman

  THE WORLD TRADE ORGANIZATION Amrita Narlikar

  WORLD WAR II Gerhard L. Weinberg

  WRITING AND SCRIPT Andrew Robinson

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  GOETHE Ritchie Robertson

  ENVIRONMENTAL POLITICS Andrew Dobson

  MODERN DRAMA Kirsten E. Shepherd-Barr

  THE MEXICAN REVOLUTION Alan Knight

  HISTORY OF CHEMISTRY William H. Brock

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  Nicholas P. Money

  Fungi

  A Very Short Introduction

  Great Clarendon Street, Oxford, OX2 6DP, United Kingdom

  Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries

  © Nicholas P. Money 2016

  The moral rights of the author have been asserted

  First edition published in 2016

  Impression: 1

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  Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016, United States of America

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  Library of Congress Control Number: 2015945428

  ISBN 978–0–19–968878–4

  ebook ISBN 978–0–19–100259–5

  Printed in Great Britain by Ashford Colour Press Ltd, Gosport, Hampshire

  Links to third party websites are provided by Oxford in good faith and for information only. Oxford disclaims any responsibility for the materials contained in any third party website referenced in this work.

  Contents

  Acknowledgements

  List of illustrations

  1 What is a fungus?

  2 Fungal diversity

  3 Fungal genetics and life cycles

  4 Fungal mutualisms

  5 Fungi as parasites of plants

  6 Fungi and decomposition

  7 Fungi in animal health and disease

  8 Edible mushrooms and fungal biotechnology

  Further reading

  Index

  Acknowledgements

  The author wishes to thank Anna Heran, Curator at the Lloyd Library and Museum, for her expertise in scanning original sources from the outstanding collection of mycological books and periodicals in Cincinnati. Additional work in preparing the figures for publication was performed by the author’s research collaborators, Maribeth Hassett, Miami University, and Mark Fischer, Mount St. Joseph University. The manuscript was proofread by Allison Davis, who was very effective in identifying topics that deserved clearer elucidation.

  List of illustrations

  1 Evolutionary relationships between fungi and animals

  2 Zoospores of a chytrid fungus

  © Joyce Longcore, University of Maine

  3 Scanning electron microscope images of yeast cells and filamentous hyphae

  © Kathryn Cross, Institute of Food Research, Norwich, UK, and Geoffrey Gadd, University of Dundee

  4 Diagram showing the interior of a hyphaltip

  © From M. Girbardt, Protoplasma 67, 413–41 (1969), with permission

  5 Young colony or mycelium of a fungus

  © From A. H. R. Buller, Researches on Fungi, vol. 4 (London: Longmans, Green, and Co., 1931)

  6 Stalked sporangium of the dung fungus Pilobolus kleinii

  7 Olpidium brassicae, an aquatic fungus

  © From J. Webster and R. W. S. Weber, Introduction to Fungi, 3rd edition (Cambridge: Cambridge University Press), with permission

  8 Spirodactylon aureum, a zygomycete fungus that grows on rodent dung

  © From R. K. Benjamin, Aliso 4, 321–433 (1959), with permission

  9 The artillery fungus, Sphaerobolus stellatus

  © From J. H. Burnett, Fundamentals of Mycology, 2nd edition (London: Edward Arnold, 1976)

  10 Fruit bodies of an ascomycete cup fungus and a mushroom-forming basidiomycete

  © From A. H. R. Buller, Researches on Fungi, vol. 1, 6 (London: Longmans, Green, and Co., 1909, 1934)

  11 Basidiospore discharge

  © From A. Pringle, S. N. Patek, M. Fischer, J. Stolze, and N. P. Money, The captured launch of a ballistospore. Mycologia 97: 866–71 (2005), with permission

  12 Structure of the fruit body of the bird’s nest fungus Cyathus striatus

  © From M. O. Hassett et al., Fungal Biology 117: 708–14 (2014), with permission

  13 Ascospore discharge

  © Illustration by Mark Fischer, Mount St. Joseph University, Cincinnati

  14 Asexual spores (conidia) of a Penicillium species

  © Richard Edelmann, Miami University, Oxford, Ohio

  15 Sexual reproduction in baker’s yeast

  © Illustration by Mark Fischer, Mount St. Joseph University, Cincinnati

  16 The life cycle of the mushroom Coprinus comatus

  © Illustration by Mark Fischer, Mount St. Joseph University, Cincinnati

  17 Mushroom expansion in Amanita phalloides, the death cap

  © From B. O. Longyear, Some Colorado Mushrooms (Fort Collins, CO: Agricultural Experiment Station of the Agricultural College of Colorado, 1915)

  18 Mature zygospores

  © From O. Brefeld, Botanische Untersuchungen über Schimmelpilze, vol. 1 (Leipzig: Verlag von Arthur Felix, 1872)

  19 Continuum of relationships between different species

  20 Scale insect trapped on a leaf surface

  © From The Genus Septobasidium by John N. Couch. Copyright © 1938 by the University of North Carolina Press. Used by permission of the publisher. www.uncpress.unc.edu

  21 Two types of mycorrhizal association between fungi and plant root systems

  © Image provided by Paola Bonfante and Andrea Genre. Reprinted by permission from Macmillan Publishers Ltd: Nature Communications, 2010

  22 The complex life cycle of a cereal rust

  23 The powdery mildew fungus Microsphaera penicillata

  © From L. R. Tulasne and C. Tulasne, Selecta Fungorum Carpologia, vol. 1 (Paris: Imperatoris Jussu, In Imperiali Typographeo Excudebatur, 1861)

  24 Appressorium of the rice blast fungus

  © From N. P. Money,
Mr. Bloomfield’s Orchard: The Mysterious World of Mushrooms, Molds, and Mycologists (Oxford: Oxford University Press, 2002)

  25 Aquatic spores produced by Ingoldian fungi

  © From J. Webster and R. W. S. Weber, Introduction to Fungi, 3rd edition (Cambridge: Cambridge University Press), with permission

  26 Ophiocordyceps unilateralis on rainforest ant

  © From L. R. Tulasne and C. Tulasne, Selecta Fungorum Carpologia, vol. 3 (Paris: Imperatoris Jussu, In Imperiali Typographeo Excudebatur, 1865)

  Chapter 1

  What is a fungus?

  Defining the fungi

  Fungi are peculiar organisms. They do not seem to move, their fruit bodies pop up overnight, and they have no visible means of feeding themselves. Early botanists considered the immobility of mushrooms as a sign of simple plant life, which explains why mycology—the study of fungi—is included in the traditional purview of botany. In contrast to plants, however, fungi do not have chlorophyll, lack leaves and roots, and never form flowers, fruits, and seeds. The combination of these non-animal and non-plant characteristics with the poisonous and hallucinatory nature of some mushrooms explains why fungi have been associated with witchcraft and supernatural beliefs. No other part of biology has encouraged this kind of folly. Putting aside the paranormal, this short book concentrates on the remarkable facts of fungal biology and the global significance of these enchanting organisms.

  Until the 17th century, natural historians had no understanding of fungi beyond what little had been gleaned from looking at mushrooms and considering their edibility. This changed with the invention of the microscope and Robert Hooke published striking drawings of fungi sprouting from a ‘mildewed’ book cover and infecting the leaves of a rose bush in his famous Micrographia (1665). Hooke was uncertain about the identity of fungi, describing the anatomy of mushrooms in the section of his book on sponges. Later investigators were fascinated by the movement of fluid they observed inside fungal cells and wondered whether these lively filaments were produced by a strange group of animals. Linnaeus found the fungi very perplexing and classified them with worms in the 1767 edition of his Systema Naturae, but the long-standing consideration of fungi as primitive plants survived this zoological interlude.

  The modern scientific definition of the fungi draws upon information from a variety of sources. Three principal characteristics unite the fungi: they are eukaryotes, which feed by absorption, and reproduce by forming spores. The term ‘eukaryote’ refers to cell structure and means that an organism’s genetic information is housed inside a structure called a nucleus. Animals and plants are eukaryotes too, along with single-celled amoebae, microscopic algae, slime moulds, and seaweeds. Other forms of life—bacteria and archaea—are prokaryotes that do not have nuclei. Fungi feed by digesting materials produced by animals and plants. They do this by releasing enzymes that break down complex substances into smaller molecules including sugars, amino acids, and fatty acids, which are transported into the cell. This feeding mechanism is referred to as ‘osmotrophy’. We perform a similar process when we use our digestive enzymes to break down carbohydrates, proteins, and fats in our digestive system. Spore formation is the third unifying characteristic of fungi. Fungi produce an awful lot of spores: a single mushroom can release 30,000 spores per second from its gills and millions of tons of these tiny particles are dispersed in the atmosphere every year.

  Genetics and evolutionary origins

  In addition to the trinitarian description of fungi as eukaryotes that feed by absorption and reproduce by spore formation we can separate them from other forms of life using genetic and cell biological criteria. Comparisons between key genes in different organisms—revealed in strings of the universal four-letter DNA alphabet (A, T, G, C)—provide a powerful measure of relatedness. The sequences of these genes in species of fungi that form the fly agaric mushroom (red cap with white spots, Amanita muscaria) and the death cap mushroom (greenish cap, Amanita phalloides) are more similar to each other than the sequence of either mushroom is to the DNA of baker’s yeast (single-celled fungus, Saccharomyces cerevisiae). If we compare the genes of all three fungi with the sequences of the same genes in fish or humans, it is apparent that the mushrooms and yeast are more similar to one another than any of them is to an animal (Figure 1). This finding reflects the relatedness of the fungi and their separation, over the course of hundreds of millions of years, from the animals. This use of genetics to reveal evolutionary kinship between organisms is the science of molecular phylogeny.

  In practice, it is quite difficult to study the evolutionary relatedness of organisms as distant as mushrooms and animals because genes that are useful for comparing different fungal species do not work as well for animals. Nevertheless, these big picture studies of evolution show, in fact, that fungi are more closely related to animals than they are to plants. According to the current view of biological diversity, fungi and animals occupy one of the seven or eight major branches of eukaryote life. Each of these branches is given the name of a taxonomic supergroup and the fungi and animals belong to the Opisthokonta supergroup.

  1. Evolutionary relationships between fungi and animals illustrated in a horizontal ‘tree’.

  The name opisthokont refers to the formation of cells that swim using a single posterior tail or cilium. Human sperm cells move in this fashion and aquatic fungi called chytrids use the same propulsive mechanism. Most fungi do not produce cilia, but their presence in chytrids, which are viewed as relatives of the earliest fungi, is seen as strong evidence of the common ancestry of fungi and animals (Figure 2). Biologists have designated Kingdom Fungi and Kingdom Animalia as distinct groups within the supergrouping of the Opisthokonta.

  The emergence of the fungi as a distinctive group of organisms is estimated to have happened between 760 million years ago and one billion years ago. This fuzzy Precambrian origin, somewhere in the early Neoproterozoic Era, is inferred from genetic differences between living fungi. Estimates of the rate of change of genetic sequences serve as a ‘molecular clock’ for calculating the time when particular groups of organisms diverged from one another. Fossils of fungi are helpful for calibrating these clocks. These include tiny mushrooms preserved in 100 million-year-old Cretaceous amber, colonies of fungi related to chytrids in 400 million-year-old Devonian chert, and large spores in 460 million-year-old rocks deposited in the Ordovician.

  2. Zoospores of a chytrid fungus. Each spore has a single flagellum.

  The Cretaceous mushrooms are beautifully preserved, but their resemblance to fruit bodies that we find in the woods today shows that this group of fungi evolved much earlier. This conclusion is supported by the discovery of 330 million-year-old fossils of the type of cells that that are characteristic of mushroom colonies. The chytrid relatives are more interesting because they show that fungi were flourishing alongside diverse plant communities that spread across the Devonian landscape. The shape and size of the Ordovician spores suggests that they were produced by a species belonging to a group of fungi that form associations with plants called arbuscular mycorrhizas. This suggests that early fungi were engaged in supportive partnerships with the first land plants. Together, these precious fossils demonstrate that fungi and plants have occupied the same habitats for almost half a billion years.

  The fungal cell

  The Precambrian separation of the fungi and the animals was probably driven by their pursuit of different ecological opportunities and this evolutionary divergence led to the development of features of cell biology and physiology found only in fungi. These exclusive characteristics are layered upon the essentials of eukaryote structure and function that include the expression of genes contained in a nucleus and power generation by organelles called mitochondria.

  The fluidity of fungal membranes is maintained by a lipid molecule called ergosterol. Cholesterol does the same thing in animal membranes and the absence of ergosterol in humans makes it a good target for drugs used to treat fungal infections (Chapter
7). The lipid membrane of fungi is surrounded by a cell wall whose chemical composition distinguishes fungi from plants and other organisms with cell walls. Plant cell walls contain cellulose. Fungal walls contain chitin, chains of sugar molecules called glucans, and mixtures of proteins. Chitin, which forms the exoskeleton of insects and is widespread in other animal groups, is made from chains of two kinds of modified sugars called amino sugars. The chitin content of the fungal wall can be quite low compared with the glucans, but chitin forms long strands that have tremendous tensile strength. The wall needs to be strong because the cell contents are inflated to the same level of pressure as bicycle tyres—albeit with compressed fluid rather than air—and rupture if the wall becomes weakened. This ‘turgor pressure’ is an important characteristic of fungi and its role in growth is described later in this chapter.

  Like other eukaryotes, the inside of the fungal cell (the cytoplasm) contains compartments surrounded by membranes that form a series of globules that transfer materials between the cell and the environment. This endomembrane system includes the endoplasmic reticulum, Golgi apparatus, elongated vacuoles, and small spherical vesicles. One of the main functions of the endomembrane system is to deliver new membrane and cell wall components to the growing cell surface. The growth process is also dependent on the arrangement of an internal framework of protein strands. This cytoskeleton is constructed from microfilaments of the protein actin and hollow microtubules of tubulin. Microfilaments and microtubules serve as tracks for molecular motors (natural nanomachines) that ratchet along their surface carrying endomembrane vesicles around the cell.

  This essential set of structures is found in two kinds of fungal cells: filamentous hyphae, which grow by elongation and branching, and yeasts that multiply by forming buds (Figure 3). The cytoskeleton inside a hypha is organized lengthwise such that vesicles delivering new cell materials from the endomembrane system are transported towards the growing tip of the cell. When the vesicles reach the end of the cell they fuse with the membrane, allowing it to expand. The turgor pressure within the cell tends to smooth the expanding membrane and extend the cell wall. This pressure results from the absorption of water by the cytoplasm. Growth is not simply a matter of pressurized inflation, however, because there is a complex interplay between the level of turgor in the cell and the mechanical properties of the cell wall. The hypha controls the fluidity of its wall with great finesse, loosening the chemical bonds between the chitin and glucan molecules, allowing them to slip past one another without triggering the explosion of the cell.