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Diseases of Fungi

Introduction

Any production system that uses an organism of a single genotype under highly intensive conditions is at a very high risk of significant disease. Viruses and other genetic elements are common inhabitants of fungi. As viruses have a small genome, increased virulence resulting from a chance mutation is likely. Some of the principles of this page apply to all microbes associated with the host, and some are specific to viruses.

Most viruses detected in fungi contain double stranded (ds) RNA. A few positive single strand RNA viruses have been characterised. No negative single strand RNA or single strand DNA viruses are known. A protein coat may envelope the virion (nucleic acid). Further, some encapsulated virions are wrapped in a membrane of host origin. Some potential viruses might also be considered as transmissible genetic elements, and given a different name. Care must be taken when reading the literature on fungal viruses.

Viruses are thought to be ubiquitous in fungi. Estimates of their presence suggest that 80% of species may be colonised. Most viruses have not been associated with any form of noticeable pathology, or expression of phenotypic change, and are thought to be benign or latent (see below for some examples). All viruses have been found within fungi and their existence outside the fungal host is unknown. The lack of an extracellular phase has implications for transmission.

Transmission

In those few associations where transmission has been studied, the virus is transmitted vertically or horizontally, or both.

Vertical transmission refers to the movement of virions into the reproductive units of the fungus, to then be expressed in the next generation. The virion is carried in the spores. Following germination of the spore, the virus appears in the next generation.

Horizontal transmission is where anastomosis between compatible hyphae results in the movement of cytoplasm containing the virions to the uninfested mycelium. The importance of vegetative compatibility cannot be overemphasised. Compatibility determines the potential for transmission, and is thus enormously important in the ecology of the virus, especially when infection is associated with disease. LINK

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La France Disease of Mushrooms

Cultivated mushrooms have been examined for viruses especially after reductions in productivity. Several different viruses appear to be pathogens; La France disease has been most widely studied.

The presence of an isometric particle has been consistently associated with the disease. Infected cultures grow more slowly. Basidiocarps of infected tissue appear earlier, they are smaller and commonly deformed. Total spore production is reduced though spores appear sooner. The disease is highly infectious, and rapid spread through a production system, and between adjacent farms, is possible.

The virus can be spread vertically and horizontally. Vertical spread is associated with the early appearance and release of spores from infected mushrooms. These spores anastomose with uncontaminated hyphae and transfer the virus. The virus multiplies rapidly and spreads through the contiguous mycelia.

Horizontal transmission means that only a small amount of contaminated mycelia mixed in with spawn may result in the entire bed rapidly becoming infected. Hyphae grow and establish anastomoses with compatible hyphae (most likely all the bed).

Transmission between farms is possible if they are using fungi with compatible hyphae. This is the case when farmers are using a single variety of fungus. Use of different varieties reduces the chance of transmission. However, even unrelated varieties may have a low level of compatibility, thereby enabling the occasional anastomosis and transmission of the virus. Complete incompatibility is uncommon, so virus transmission remains a potential problem for all mushroom farms. LINK

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Killer Yeasts

Killer Yeasts are strains that are infected with one of a group of viruses that produce a toxic protein that kills closely related but uninfected yeasts. The yeasts belong to a wide diversity of fungi, including the bread-making and alcohol-producing Saccharomyces cereviseae and the maize smut Ustilago maydis. Killer yeasts are tolerant of the toxins they produce, but may be susceptible to toxins of different Killer yeasts. The genes that confer toxin production and resistance to the toxin appear to be on the virus genome. However, replication and other functional genes of the virus may be on the host nucleus.

The fitness of Killer yeasts in natural habitats is partly attributed to their toxin production. LINK The toxin apparently regulates competition and enables the host cell to proliferate.

Killer yeasts are commonly found on fruits such as grapes and flowers. The killer yeasts are important for fermentation of grapes, because they may slow fermentation and leave undesirable flavours in the wine. Killer yeasts can take over fermentation by killing the inoculated yeasts, even when the concentration of killer cells is low at the beginning of the process. The potential of Killer yeasts is being examined for commercial exploitation. The capacity to add desirable fermentation characters to strains that already reduce competitors in the must is a valuable attribute. Use of killer strains may reduce the need to sterilise must at the beginning of fermentation. LINK The sterilant, sulphur dioxide, induces asthma and allergic sinus conditions in some individuals, and is therefore seen as an undesirable though necessary additive to wine.

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Response of the Fungi

Pathogenic viruses are found where the fungal population is held at artificially high levels by human intervention. This has led to the suggestion that most viruses are naturally benign. However, the absence of fungi may be associated with the action of pathogens: we have too little information.

Viruses have become pathogens because chance mutations in the small genome occur at a much faster rate than in the host, and selection is for pathogens when host populations are held at high densities. In other words, disease is a function of the attempts by humans to manipulate the environment.

The fungus is not a passive player. Like most eukaryotic organisms, fungi have RNA silencing. RNA silencing is where dsRNA is recognised. The RNA is cleaved by a RNAase called "dicer" into lengths between 19 and 25bp. These are neutralised. Some fungi have more than one recognition system, each acting at different stages of the life cycle. Indeed, silencing defective mutants of fungi have quite unexpected functional attributes. It appears dsRNA viruses have been associated with fungi for a long time.

However, the presence of Killer yeasts indicates that the interaction between virus and fungus may be more complex. Where the virus provides a beneficial function for the host, then the virus or parts of its genome may become incorporated into the host genome. Competitors may be almost entirely replaced in a population.

Thus viruses are not one functional grouping. They have attributes determined by their genome, and we will no doubt find further variants as fungi are used more extensively and intensively.

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Conclusion

The vast majority of viruses of fungi have no noticeable effect on host phenotype. In those that modify host function, some are deleterious and others beneficial. Because viruses can be transmitted following compatible anastomoses, single genotypes remain potentially at risk of rapid spread of disease (in industry). Lack of transmission across incompatible strains limits their use in biological control of problem fungi.

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References

Milgroom M.G. (1999) Viruses in Fungal Populations, in Structure and Dynamics of Fungal Populations ed J. Worrall, Kluwer, Dordrecht.

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