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Peter Flegg Investigates: A mushroom mystery – Mummy
This article is reprinted from the August edition of The Mushroom Journal, the journal of the MGA. Peter Flegg is the Editor of that journal as well as the newsletter of the International Society for Mushroom Science.
Peter started with the Mushroom Research Association (MRA) as a chemist in 1950 and transferred to the Glasshouse Crops Research Institute (GCRI) in 1954, continuing his work on mushrooms. He studied with Dr. Lambert at the USDA in 1962 on a Kellogg Fellowship and then returned to GCRI, becoming the head of the mushroom section in 1975 and continued to work on many aspects of mushroom biology and cultivation until his retirement in 1983. Peter published many articles and scientific papers while at GCRI and after his retirement remained active in the industry as a consultant and technical writer. He took over as Technical Editor of The Mushroom Journal in 1981 and as Editor this year. He has been the Editor of the ISMS Newsletter since 1989.
It seems logical. Every disease has a cause. Mummy disease should therefore be no exception, but, so far, there appears to be no one single identifiable causal agent. Several scientists, between them, have put forward a number of possible organisms on which to lay the blame. Surely, one may think, with a number of suspects lined up, it ought not to be too difficult to decide which is the culprit. Well, there are rules which are used to decide these things. It’s not a matter of setting up a panel of experts to hear the evidence and vote.
The rules in an early form were put forward about 150 years ago by Jacob Henle at G�ttingen University. It was one of his students, Robert Koch, later held to be one of the greatest bacteriologists ever known, who developed these rules into the form they are known and followed today. It was he who identified the three separate species of bacteria causing anthrax, tuberculosis and cholera. Professor Koch was awarded the Nobel Prize for Medicine in 1905.
In essence his four rules for deciding on which organism is the true cause of a disease are:-
1. In all cases a specific organism must be identified.
2. It must be obtained in a pure culture.
3. Organisms taken from the pure culture must consistently reproduce the disease they are suspected of causing in experimental animals (or plants).
4. The organism must be recoverable from the diseased plant or animal.
Clearly, to see what organism can be isolated from a sick plant or animal and blame that organism for the disease just won’t do. It has to be shown that the suspect is capable of causing the same disease it is suspected of causing - not just any old disease but the one causing the initial symptoms.
The rules are quite strict but they do ensure that disease and causal agent are properly linked.
Mummy disease - symptoms
One of the troubles with mummy disease is in trying to fulfil the requirements of these rules. There are several suspects but the evidence is not absolutely convincing.
Another trouble is that we cannot be sure that all the symptoms ascribed to mummy disease really are those of genuine mummy.
The disease was first described in 1942 by CM Tucker and JB Routien in the United States (Missouri Agricultural Experiment Station Research Bulletin, 358). This is not available to me, but there is an early account of the disease by C Fleury in the MGA Bulletin No. 22 (January 1951). He describes an outbreak which occurred in Switzerland and both refers to the earlier American work and reproduces some of the photographs from it.
Among the main symptoms described are an early cessation of growth and cropping, fruit bodies with tilted caps, veil breaking early, the base of the stem enlarged and the stalk curved. The tissue of the mushroom becomes spongy, dry and brown giving a mummified appearance.
A particular feature of this disease is its rapid rate of spread through the bed, up to 30cm (12 inches) daily has been reported.
Pickers are said to be able to detect this disease while harvesting the crop because of the tough and dry texture of the mushroom tissue which has a "gritty" texture when cut. Sometimes there is evidence of brown streaks, a water-soaked appearance and cavities in the mushroom tissue. Fred Atkins (Mushroom Growing Today, 1966 Edition) gives the disease the two alternative and descriptive names "Crook Neck" and "Wormhole Disease".
The caps and stem are reported by some to break with a distinctive "snap".
When pulled from the casing a large amount of casing is left adhering to the base and the mycelium has been described as "stringy".
Most writers on the subject include most of the symptoms already described, but a little uncertainty must creep in as the cause of the disease has not yet been definitely established.
Mummy disease - causes
The authors who first described the disease plumped for it probably being caused by a virus. Fleury’s early experience was similar to that of the Americans, in that several kinds of bacteria could be isolated from the diseased mushrooms but when healthy mushrooms were subsequently infected with cultures of these bacteria, black spots developed on the mushrooms but with no sign of mummy disease. The bacteria were probably acting as a secondary infection on the already diseased and weakened fruit bodies.
During the late 1950s Kneebone and his students at Penn State University made several studies of mummy disease (Mushroom Science 4, 1959). They described the symptoms as similar to many of those already mentioned but were unable to fulfil Koch’s rules for determining the cause of the disease. However, they were able quite easily to transmit the disease by transferring diseased compost and casing containing mushroom mycelium to healthy crops. To transfer mummy disease successfully it was necessary for the diseased mushroom strain, to be compatable with the healthy strain, that is, the strains had to be able to anastomose to enable the disease agent to pass from one mushroom strain to another. This suggested that the disease agent was inside the mycelium.
While studying the bacterial diseases of mushrooms Doreen Gandy (GCRI Annual Report for 1968) isolated a bacterium from mummy-diseased mushrooms which was similar to the bacterium Pseudomonas tolaasi (P. fluorescens) which causes bacterial blotch. This was also the experience of Schisler, Sinden and Sigel in 1967 (Phytopathology 68, 944-948). This bacterium from mummy-diseased mushrooms, unlike the blotch-causing bacterium, was able to develop blue and bright yellow pigments in the culture media it was being grown in. Doreen identified this organism as Pseudonomas aeruginosa which, while not reproducing mummy disease symptoms, did severely restrict the growth of mushroom mycelium.
Here indeed was a mushroom mystery. In the early days mummy disease in some ways appeared similar to and was probably confused with another mystery disease which was, then, variously called X-disease, Brown disease, Watery-stipe, La France disease and Die-back. However, unlike the latter collection of "diseases", which were clearly shown in 1962 to be caused by a number of viruses, mummy disease retains a considerable portion of its mystery.
Several years of research into this mysterious disease done during the 1970s at the Horst Mushroom Experimental Station were described by Annemarie Van-Zaayen in, for example, the Mushroom Journal No. 102 in 1981.
She found the typical symptoms of mummy and commented on the early confusion with virus disease. Electron microscopy showed that sections of mummy-diseased mushrooms contained mushroom cells with bacterial cells within them. This rather confirmed earlier observations in the United States and elsewhere. Van-Zaayen and her colleagues examined the bacterial cultures obtained by Schisler and colleagues earlier but were unable to establish whether the American isolates were really the cause of mummy. It seemed that the mummy disease bacteria lost their ability to infect the mushroom. Infection tests with their own isolates in the Netherlands did not go smoothly either. Efforts to produce the symptoms of mummy disease in mushrooms gave very unreliable results.
Clarification and complication
More recent work, Betterley and Olson, 1989 (Mushroom Science 12) and Wuest and Zarkower, 1991 (Mushroom Science 13) has both clarified and complicated the mystery.
Betterley and Olson found several isolates of bacteria in association with mummy disease and were able to classify most of them as a sub-group of Pseudomonas fluorescens biotype G (= Biovar V). They were also able to infect mushrooms, to obtain mummy symptoms and to recover the bacteria.
On the other hand, several workers have, over the years found Pseudomonas aeruginosa to be associated with mummy disease and Wuest and Zarkower decided on a more thorough study of it. Their experiments certainly implicated P. aeruginosa as a pathogen and suggested that mummy disease could be caused by at least two different species of bacteria, the one named by Betterley and Olson and P. aeruginosa. They also drew attention to a report by Fletcher of a disease with similar symptoms to those of mummy. Features which distinguish Fletcher’s crypto-mummy, as he calls it, from mummy are its lack of rapid spread and that the mushroom crop can recover to produce healthy mushrooms. Crypto-mummy, it seems, is often associated with chronic over-watering of the crop.
By way of explaining the difficulties and uncertainties of producing mummy disease with pure-culture bacterial suspensions, Wuest and Zarkower pointed out the considerable effect that the bacterium P. aeruginosa can have on the other microbes in the compost. It is very active in repressing the growth of many normal inhabitants of the compost (including the mushroom - remember Doreen Gandy’s work?). They suggested that the dominance of this bacterium wherever mummy disease occurred should be studied further.
If, by now, you are feeling that the identity of the causal agent of mummy disease is surrounded by more than a modicum of uncertainty, then, I cannot disagree with you.
Mummy disease - control
The most common recommendation for the control of mummy, and it can only really apply to shelf beds, is to dig a trench (or trenches if the disease is moving in both directions along a shelf). The aim of trenching is to separate the diseased area from the healthy. Because of the rapid rate of spread of the disease the trench is recommended to be dug around 2m (6-8ft) ahead of the advancing disease and the trench itself to be several inches wide. All compost and casing has to be removed from the trench and the gap thoroughly disinfected. The whole business of trenching sounds a potentially messy one to me.
When the crop is being grown in separate containers, eg trays or bags, the usual advice is to isolate or dispose of them. Whichever method of control is used, good hygiene is strongly recommended.
As Fred Atkins wrote of mummy disease many years ago, "there is no cure", true then and true now.It is altogether not a very comfortable situation. I am not sure what Professor Koch would have made of it, but the moderately good news is that mummy disease does not often seem to be a major cause of crop loss.