21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 15: Fungi as symbionts and predators of animals
2. Chapter 16: Fungi as pathogens of animals, including man
   1. Pathogens of insects
   2. Microsporidia
   3. Trichomycetes
   4. Laboulbeniales
   5. Entomogenous fungi
   6. Biological control of arthropod pests
   7. Cutaneous chytridiomycosis: an emerging disease of amphibians
   8. Aspergillosis disease of coral
   9. Snake fungal disease
   10. White-nose syndrome of bats
   11. Mycoses: the fungus diseases of humans
   12. Clinical groupings for human fungal infections
   13. Fungi within the home and their effects on health: allergens and toxins
   14. Comparison of animal and plant pathogens and the essentials of epidemiology
   15. Mycoparasitic and fungicolous fungi
   16. Chapter 16 References and further reading
   17. Buy a PDF of Chapter 16
3. Chapter 17: Whole organism biotechnology

16.14 Comparison of animal and plant pathogens and the essentials of epidemiology

We have shown in this and earlier Chapters that fungi are important pathogens of both plants and animals and you may well have detected some similarities in the concepts and themes that we have described under these topics. It is worth attempting a summary comparison (Sexton & Howlett, 2006). An important difference is that:

• fungi cause more disease in plants than either bacteria or viruses;
• bacteria and viruses cause more disease in animals than fungi.

Epidemiology is the study of disease distribution in populations. As a descriptive or analytic exercise it examines (often historically) how a disease affects a population; as an activity it may attempt to control the spread and severity of diseases. There is a human-centric tendency in epidemiology: for the most part animal epidemiology is a branch of medicine concentrated on human diseases, and the epidemiology of plants is concentrated on agricultural and horticultural crops.

Without always labelling it as such, we have already dealt with the epidemiology of many fungal infections. For example, we have already made it clear (Section 16.12) that species of Candida and Aspergillus are the most common causes of invasive fungal infections of humans, although several other fungi are emerging as significant opportunistic pathogens (Pneumocystis, Zygomycetes, Fusarium spp.). Similarly, several examples have been given of factors affecting the spread and management of plant disease in the field and the impact of epidemiological knowledge on plant disease management (Chapter 14).

As we have seen in this Chapter, fungal pathogenicity in (vertebrate) animals depends on the immune status of the host. The decisive significance of the immune system in controlling fungal infection, particularly in humans, is demonstrated by the devastating impact of common saprotrophic fungi as opportunistic fungal pathogens in immunocompromised patients described above. Plants do have defences, but plant cells do not move. A crucial element of the vertebrate immune system is the recruitment (that is the movement) of cells towards the point of challenge. A plant cannot reinforce its defences in this way so the challenge is between an invading hypha and one defending plant cell. The best defence that a plant can achieve is the programmed death of challenged cells represented in the hypersensitive response that confers resistance to biotrophic pathogens (see the section entitled Enzymatic penetration of the host in Chapter 14; CLICK HERE to view the page).

Aside from these biological differences, there are some technical factors that constrain any comparison of fungal pathogenesis in plant and animal hosts:

• plants can be manipulated without the ethical issues associated with animal experimentation;
• experimental study of human-pathogenic fungi generally relies on cell lines and experimental animal models, plant pathogens can be studied directly on their hosts;
• because many more fungi infect plants than animals, a larger number and wider range of plant-fungus systems than animal-fungus systems have been studied.

There is a further problem in that the word virulence has a slightly different technical meaning to animal and plant pathologists. In plain English virulence refers to the ability of a microbe to cause disease; it is often used interchangeably with the term pathogenicity although virulent often implies that the pathogen does a lot of damage to the host. Unfortunately, the ‘gene for gene’ theory of how plants recognise and respond to fungal pathogens, suggests that two genes, one in the plant and one in the fungus, are involved and introduced the term avirulence gene to describe the fungal gene whose product is identified by the plant’s resistance gene (see the section entitled Genetic variation in pathogens and their hosts in Chapter 14; CLICK HERE to view the page). The plant genes act as the plant equivalent of the animal immune system by recognising components of the pathogenic fungus to which they can react to prevent the infection. Animal biologists already have a term for the immune interaction; they call the identifying material on the infective agent an antigen.

• So for an animal pathologist a virulence gene in an infective agent produces the antigen that challenges the host;
• for a plant pathologist a virulence gene is an allele of an avirulence gene and does not produce the product that promotes plant resistance.   

The complex interactions involved in fungal diseases of plants have been rationalised using the concept called the ‘Disease Triangle’ (see the section entitled Plant disease basics: the disease triangle in Chapter 14; CLICK HERE to view the page), which places the three factors which must interact to cause plant disease at the three corners of a triangle. Those three factors being:

• a susceptible host,
• a disease causing organism (the pathogen)
• a favourable environment for disease.

A similar concept developed for animal pathogens more recently is the ‘damage-response’ framework described by Casadevall & Pirofski (2003), which emphasises that the outcome of an interaction is determined by the amount of damage incurred by the animal host. This is an attempt to make the concept more realistic by reconciling ‘microorganism-centred’ and ‘host-centred’ views of microbial pathogenesis to focus experimental studies around a common principle. The basic tenets of the damage-response framework are that:

• microbial pathogenesis is an outcome of an interaction between a host and a microorganism,
• the host-relevant outcome of the host-microorganism interaction is determined by the amount of damage to the host,
• host damage can result from microbial factors and/or the host response.

Very few fungi can infect both animal and plant hosts, so comparisons have to be made between different species. Most is known about fungal pathogens that belong to the Ascomycota. Certainly among v,ertebrate animal pathogens there is only one known chytrid disease (of amphibians), and relatively few diseases of humans caused by zygomycetes or Basidiomycota. Even though, as discussed above, zygomycosis and cryptococcosis are clinically important diseases, they represent too few examples of animal fungal diseases for much worthwhile comparison to be made with the many plant diseases caused by members of these groups. Consequently, we will limit this discussion to Ascomycota, and immediately highlight a point of difference in that animal and plant pathogens are concentrated in different classes among the Ascomycota (CLICK HERE to download our Outline Classification of Fungi as a PDF file):

• the classes Leotiomycetes, Dothideomycetes, Sordariomycetes, and Taphrinomycetes are rich in plant pathogens;
• whereas animal pathogens belong to the class Eurotiomycetes (in the subclasses Chaetothyriomycetidae and Eurotiomycetidae) that contains few plant pathogens (Berbee, 2001).

There are surprisingly few publications that discuss comparatively fungal pathogenesis in animals and plants; we can draw your attention to Hamer & Holden (1997), Sexton & Howlett (2006) and Casadevall (2007). Sexton & Howlett (2006) describe parallels in fungal pathogenesis of plant and animal hosts, focusing on the Ascomycota. In brief those comparisons are placed in seven stages:

• Stage 1, attachment of conidia and or ascospores, in plant pathogens, or yeast cells, hyphae, or arthrospores in animal pathogens to a surface and recognition of the host.
• Stage 2, activation of the infecting fungal propagule.
• Stage 2a, germination of ascospores (plant pathogens), conidia, or arthrospores.
• Stage 2b, dimorphic switching of animal pathogens from a yeast phase to a pathogenic hyphal stage or from hyphae to a pathogenic yeast phase.
• Stage 3, penetration of the host may involve mechanical pressure, such as that produced by appressoria in some plant and some insect pathogens; lytic enzymes, such as proteases; and additional cell wall-degrading enzymes, including cutinases, cellulases, pectinases, and xylanases in plant pathogens; protease followed by chitinase is needed to dissolve the insect cuticle. Natural openings in the host, such as stomata in plants or wounds in animals and plants, are also entry points for pathogenic fungi.
• Stage 3a, some animal pathogens (for example Histoplasma capsulatum) use receptors on the host cells to bind and facilitate endocytosis as a means of penetrating the host cells.
• Stage 4, avoidance of host defences. Pathogenic fungi may detoxify oxidative molecules such as superoxide and antifungal compounds and synthesise protective molecules such as melanin. Animal-pathogenic ascomycetes often avoid or inhibit animal immune system components. Plant pathogens may avoid exposure to fungal wall-degrading enzymes by causing little host cell damage when undergoing intercellular biotrophic growth or by producing inhibitors of these plant enzymes.
• Stage 5, colonisation of the host environment, which often results in host cell death, may require specific nutritional mechanisms such as those for iron uptake in animal hosts, and can produce other changes in host physiology, such as the pH level, to create a more favourable environment for the pathogen.
• Stage 6, asexual reproduction in the pathogen.
• Stage 6a, asexual reproduction often results in conidia emerging from lesions on the host surface of plants.
• Stage 6b, spore formation in the host is less common in vertebrate animal pathogens, and direct host-to-host transmission is rare. Coccidioides immitis produces endospores in host tissue by numerous mitotic divisions inside a spherule. Remember that copious asexual spore formation is common in invertebrates, particularly following death of the (arthropod) host.
• Stage 7, sexual reproduction. Mating and meiotic division produce ascospores during the disease cycle of plant-pathogenic fungi. This can result in recombinant offspring if mating occurs with a genetically different individual (obligatory in heterothallic but not in homothallic fungi). Sexual reproduction has not been reported to occur in animal-pathogenic fungi, with a few possible exceptions, such as Pneumocystis spp (Sexton & Howlett, 2006).

Overall, there are clear similarities, particularly in terms of the ability of fungi:

• to adhere to the host,
• to use their filamentous hyphae to penetrate the host, and then to
• use their ability to secrete a comprehensive panel of enzymes to digest and use components of the host as nutrients.

There is one remaining point that this comparison does not address: namely, that fungi also parasitise other fungi. As fungi and animals are each other’s closest relatives, this seems like a reasonable place to deal with this topic.

Updated July, 2019