Bacterial soft rot in mushrooms, an overview

Bacterial soft rot in mushrooms only has a brief history in mainland Europe. With the exception of a few sporadic incidences in French caves (Olivier, 2001, oral report) this phenomenon was unknown to our growers until recently. In the UK however, this disease has already been causing trouble for some time.  The first literature devoted to soft rot in Agaricus bitorquis dates from the early 1990s (Lincoln et al., 1991).  Reports of outbreaks in Agaricus bisporus only appeared a few years later. The first report in Belgium dates from 2000 (Anonymus, 2000).  In the Netherlands the first report dates from 2001 (Hesen, 2001, oral report).
Until now two pathogens of soft rot have been identified - Burkholderia gladioli pv. agaricicola and Janthinobacterium agaricidamnosum.

B. Desrumaux, experimental centre for mushroom cultivation,
Rumbeke, Belgium

Burkholderia gladioli pv agaricicola

Scientific name: Burkholderia gladioli pv agaricicolasyn.

Syn. Pseudomonas gladioli pv agaricicola Severini

Dutch               Bacterial zachtrot

French              Pourriture molle - putréfaction molle

English             Soft rot

German            Weichfäule

Host mushroom

The B. gladioli-softrot problem mainly occurs in mushrooms cultivated in the tropics and sub-tropics. As it is generally only Agaricus bitorquis that is grown in these conditions, the problem in practice mainly focuses on this mushroom variety (Atkey et al., 1991). This does not mean that B. gladioli will not infect Agaricus bisporus too, if it is also grown under these higher temperatures (Fermor & Lincoln, 2000).

Development and symptoms

Research (Atkey et al., 1991) shows that approximately 13 hours after infection with B. gladioli the first (microscopic) sunken lesions appear on the mushroom cap. Until that moment no depth effect of the bacteria was visible. About 21 hours after infection the bacteria have multiplied and the symptoms develop rapidly. At this stage it seems that any resistance is breached, so the disease develops at an accelerated pace. There are indications the bacterial presence is both extra and intra cellular. 

One day after infection a nearly 1 millimetre deep lesion is apparent. Research shows that the development of this lesion now develops horizontally instead of vertically, in other words the pitted lesion starts spreading sideways. It also appears that the epidermis of the mushroom is less affected than the layer just below. The upper skin seems to be suspended above the (undermined) sub layer. This occurrence lead researchers to conclude that the actual outer skin of the mushroom has a certain tolerance to the bacterial infection, and also that the collapse of the hypha or mycelium threads prevents the infection penetrating into the body of the fruit.

Soft rot becomes visible to growers very shortly after infection. Depending on the extent of infection, the symptoms vary from slight patches to the formation of deep lesions in the cap, and in the worst cases complete disintegration caused by the cap and stem rotting away. Mature mushrooms exhibit typical eroded patches. These lesions extend to the stem, destroying all the tissue in the process. In some cases the stem rots away entirely.  Remarkably the upper layer of the cap is often unaffected, while the underlying hypha dissolve into a sticky, brown slime (Gill & Cole, 1992).  The time taken for this rotting process to destroy the mushrooms is just 48 hours (Fermor & Lincoln, 2000).

The most conducive temperature for the development of B. gladioli is between 28 to 30 degrees celsius. The temperature used to grow Agaricus bisporus (16 - 18 degrees celsius) greatly delays infection development (Fermor & Lincoln, 2000).

Prevention and control

As Agaricus bitorquis has no longer been grown in Belgium since the early 90s and improved climate control (with cooling) means high temperatures no longer occur in growing rooms, it is highly unlikely that this form of bacterial soft rot will appear on Belgian farms. If growers of A. bitorquis are confronted by this problem, a (temporary) switch to growing A. bisporus (cultivated at a lower temperature) is advisable, obviously taking the necessary hygiene precautions into account.

Janthinobacterium agaricidamnosum

Scientific name: Janthinobacterium agaricidamnosum sp. nov.

Dutch               Bacterial zachtrot

French              Pourriture molle - putréfaction molle

English             Soft rot

German            Weichfäule

Host mushroom

The researchers linked Janthinobacterium agaricidamnosum mainly to Agaricus bisporus. The infection was first observed in the brown varieties and only later in the white varieties (Fermor & Lincoln, 2000). This does not exclude the possibility of infection in, for example, Agaricus bitorquis (Fermor & Lincoln, 2000).

Development and symptoms

According to Lincoln et al. (1999) symptom development is more or less identical to B. gladioli. The first patches, which can occur on both the cap and the stem, are often very shiny or even watery in appearance and often pitted (Desrumaux, personal experience). Fully-grown infected mushrooms usually turn brown or grey in colour and are easily distinguished from healthy or less infected examples. At a later stage the cap develops a pitted appearance caused by the disintegration of the internal tissue. As the infection develops the mushroom often exudes droplets of moisture.

Infected mushrooms are often 'isolated' between apparently healthy specimens. In the space of 48 hours from identifying the first symptoms the mushroom has turned into a stinking pile of slime. Both cap and the stem are infected. The stench can be smelt from a distance of several metres. Extraordinarily, the disease can continue to develop after the harvest: a seemingly healthy mushroom can turn into a malodorous pulp in the post harvest handling chain.

In general Janthinobacterium agaricidamnosum develops at lower temperatures than Burkholderia gladioli. The optimal development temperature is 16 to 18 degrees celsius, the maximum temperature being some 30 degrees celsius (Fermor & Lincoln, 2000). 

A well as the temperature, the relative humidity also influences development. In vivo tests with brown varieties and small hybrids (type U3) the RH influence was more noticeable in the brown varieties: symptom development was less at an RH of 85 % than at 95 % RH (Lincoln et al., 1999). The effect of RH was limited with the small hybrid, but still present. Artificial infection of harvested mushrooms with J. agaricidamnosum showed that at an RH below 71.5 % RV no symptoms developed, at 80 % spots and light necrosis, at 85 % the first typical soft rot signs materialised and at 95 % RH there were clear signs of extensive rotting (Lincoln et al., 1999).

Research at the POVLT (Desrumaux & Sedeyn, 2001b) shows that J. agaricidamnosum has an extremely variable incubation period. Infection at casing, blow down and during pinheading all resulted in the initial symptoms during the first flush. In the previous phase no symptoms were evident. The incubation time varied here from just 2 to 13 days. Infection on incubated compost show the least risk, even though symptoms did appear.  Infection during pinheading is particularly disastrous: the first symptoms appear within 2 days to be followed 2 days later by fruit bodies disintegrating into a foul-smelling, rotten slime.

Source and transmission

The initial sources of Janthinobacterium agaricidamnosum are still an unknown factor.   Relevant literature identifies water and casing soil peat as possible carriers of the bacteria, as a similar bacteria, Janthinobacterium lividum, has been found in soil and water (Lincoln et al., 1999).  The presence of J. agaricidamnosum in casing soil has not yet been established.

Employee contact, watering and insects can all transmit the disease internally on a farm (Desrumaux et al., 2004; Lincoln et al., 1999).  Experiences with the disease in practice and with other mushroom pathogens do not exclude transmission via empty containers and machinery, although there is no scientific evidence to support this theory.

Prevention and control

Outbreaks of soft rot in Belgian and Dutch crops are quite recent, and any guaranteed successful methods of controlling the disease have yet to be found. The guidelines below are based on experiences with other pathogens and the first experiences with soft rot. In the UK, where the disease is more familiar, no ideal method to keep it in check has been found either (Fermor, 2000, oral report).

- The diversity of possible carriers on and between farms emphasises the importance of strict hygiene, both during and pre-harvest. Extra attention should be paid to disinfecting containers that may circulate around various farms. Companies that harvest mechanically must ensure scrupulous hygiene as the machinery used can easily spread the disease.

- Regarding the growing room climate, the same measures can be taken as with Pseudomonas tolaasii (bacterial blotch). A high relative humidity is conducive to disease development with both organisms. Lowering the relative humidity to below 85 % can slow down the development of soft rot according to Lincoln et al. (1999).  Such a drastic RH drop will have a negative effect on both the quality and yield experienced, so a more limited reduction of RH by 1 to 2 % would seem to be a preferable measure to help control the disease.

- As humidity must be carefully managed, pay extra attention to how much water is given.  If water has been applied on the mushrooms, they must be dried artificially. If the mushrooms and the casing soil cannot be dried in time, it's advisable to delay watering. Avoiding too wet casing soils can also help control the disease.

- The effectiveness of chlorine (natrium hypochloride) in preventing soft rot is insufficient to control the problem (Desrumaux et al., 2004). Using chloride doesn't stimulate the development of J. agaricidamnosum, although this was first suggested otherwise (Fermor, 2000, orally).

- Other agents which can be used against soft rot are unknown or unrecognised.

Symptoms of soft rot caused by Janthinobacterium agaricidamnosum nearly always appear in the first flush. The photographs give an impression of how the infection develops.