Basic IPM Practices for Organic Mushroom Farms: Syzygites Disease on the Agaricus Mushroom

Background

Button mushrooms of Agaricus bisporus (Lange) Imbach are commercially cultivated under environmentally controlled conditions. Mushrooms are the most economically important agricultural crop in Pennsylvania and an important high-cash-value crop in many other states. Syzygites megalocarpus is a common pathogen found on wild mushrooms, colonizing their surfaces with a yellow "fuzz" that becomes bluish or gray as it develops. In 2011, hybrid brown mushrooms with a hairy mold were collected from a commercial mushroom farm in Chester County, Pennsylvania. Syzygites megalocarpus was isolated from the substrate and casing layer of these mushrooms and identified by morphological characteristics and molecular analysis. A fuzzy to hairlike, grayish mycelium was observed growing on mushrooms on later breaks. Growers have reported observing up to 25 percent of the production surface area being covered with Syzygites by third break. Dead or dying mushroom primordia were found on at least two farms that were growing a relatively new hybrid strain of Agaricus bisporus (Figure 1). The new brown strain hybrid is the cross of an isolate from a commercially available strain and an isolate from a wild-type brown Agaricus.

Figure 1. Syzygites growing on hybrid strain of A. bisporus. Credit: David M. Beyer and Kimberly Paley

The Fungus

Syzygites megalocarpus is currently classified in the Fungi kingdom, Mucoromycota phylum, Mucoromycetes class, Mucorales order, Mucoraceae family, Syzygites genus, and S. megalocarpus Ehrenb.: Fr species, which is the only member of the genus. Syzygites produces two types of spores, sporangiophores and zygospores (Figure 2). The sporangiophores grow out of the substrate, are branched dichotomously up to four times, and terminate in a globose, column-shaped sporangium with a dissolving wall and few spores. The sporangiospores are shaped like globes and have spines on them. The zygospores are melanized and ornamented, and produced on opposite suspensors on zygospores that branch dichotomously and end in spines that are sterile.

Figure 2. The two types of spores formed by Syzygites sporangiospores (top) and zygospores (bottom). Credit: Kimberly Paley

This fungus does not survive for long periods in culture and tends to lose viability when grown in the lab. Cultures are also very susceptible to bacterial contamination—even when the initial culture starts out clean, contamination can easily develop in the culture later. The possibility that a bacterial-fungal relationship exists in which the bacteria play a role in disease development has been suggested, but additional studies would need to confirm this.

Signs and Symptoms

On mushroom hosts, Syzygites displays a moldy, fuzzy, and hairlike appearance, starting yellow and turning bluish to greenish gray as it matures. Symptoms are pitting, discoloration, and necrosis of mushroom caps (Figure 3).

Figure 3. The signs and symptoms of Syzygites: hairlike growth on the casing and mushroom, and the necrotic discoloration of the mushroom tissue. Credit: David M. Beyer and Kimberly Paley

Syzygites may develop on postharvest mushrooms even a few days after packaging, sometimes showing up on mushrooms in stores (Figure 4).

Figure 4. Syzygites growing on postharvest mushroom after packaging (top) and from store shelves (bottom). Credit: David M. Beyer and Kimberly Paley

Growth Factors

Syzygites mycelium grows faster at 77°F (25°C) than at 60–68°F (15–20°C) and does not grow at all at temperatures above 86°F (30°C). Sporulation occurs differently at cooler temperatures when compared to warmer temperatures, and fungal growth morphology also appears quite different at cooler temperatures.

The thermal death point of Syzygites sporangiospores was determined to be around 98°F (37°C). Therefore, it is unlikely that Syzygites survives phase II pasteurization or post-crop steaming. The thermal death point for Syzygites zygospores has yet to be determined, so it may survive at higher temperatures.

Inoculation and Secondary Spread

No infection occurred on healthy mushrooms or the casing using a spore suspension or mycelium inoculation technique. Infection does occur when inoculating knocked-over mushrooms with mycelium before first break and subsequent infections spread to healthy mushrooms. After first-break mushrooms became infected, the pathogen easily began to spread across the casing, suggesting the importance of removing dead or dying mushroom tissue from the casing after harvesting to help disease control.

Under standard room air circulation, no spores were collected near infected mushrooms. Placing a small handheld fan behind the Syzygites-infected mushroom appeared to dislodge spores from the infected mushrooms and move them, which suggests that additional air velocity can dislodge and move spores around a room. This observation was also supported by room sampling with RODAC plates, where spores were found on the upper air exhaust vent in the ceiling and could not have been moved there by water splashing, equipment, or personnel.

When the room air ventilation system was on, Syzygites did not appear to spread from an infected mushroom to other areas, suggesting that the spores are not easily moved by air alone. However, it is known that watering will dislodge Syzygites spores. These spores then become airborne and are moved around a room, which may cause secondary infection. The combination of dead or dying mushroom tissue on the casing and watering infected mushrooms between breaks may explain why later breaks can become more heavily infected on a commercial farm.

Control

Although most commercially registered fungicides are somewhat effective in culture, they do not seem to control the disease on farms. Whether applied before or after infection, fungicides do not control the spread of the disease.

Management of this disease depends on removing dead mushroom tissue from the beds and the room. Dead pins, knocked-over mushrooms, and other remaining tissue should be removed as soon as harvesting is finished for each break. Syzygites will quickly colonize dead mushroom tissue, rapidly grow over the casing surface, and infect healthy mushrooms.

All mushroom debris from the harvest should be removed from the floor and under the beds. This debris is also a potential source of food for Syzygites. To make clean-up easier, some farms place boards along the bottom beds on the floor to prevent mushroom debris from getting under the beds.

Infected mushrooms should be covered with a wet (alcohol or salt water) paper towel and then covered with salt, limestone, or gypsum to contain the spores (Figure 5). These infected mushrooms should be covered before watering, and if possible, room fans should be turned off during watering and remain off for a short period of time to allow any disturbed spores to settle. Later breaks that are heavily infected should be steamed off as early as possible to prevent contamination of newer crops.

Figure 5. Covering of an infected mushroom with a wet paper towel and salt to prevent the secondary spread of Syzygites spores. Credit: David M. Beyer

Sources

Beyer, D. M., K. O’Donnell, K. Paley, and M. P. Wach. 2013. "First Report of Syzygites megalocarpus (Mucorales) Web Mold on the Commercial Portabella Button Mushroom Agaricus bisporus in North America." Plant Disease 97, no. 1 (January).

De Soto, J. G. "Etiology and Epidemiology: Interactions of Syzygites megalocarpus and Agaricus bisporus." Master’s dissertation, Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, 2018.

Prepared by David M. Beyer and Kimberly Paley.

Supported in part by a USDA NIFA grant "Collaborative Research and Extension Network Addressing Challenges for Sustainable Organic Mushroom Production," USDA NIFA Award number 2017-51300-26818, USDA National Institute of Food and Federal Appropriations under Project PEN04731 and Accession number 102319, the Mushroom Industry Endowment and the Giorgi Mushroom Funds.