Abstract
The production and culture of new species of mushrooms is increasing. The breeding of new strains has significantly improved, allowing the use of strains with high yield and resistance to diseases, increasing productivity and diminishing the use of chemicals for pest control. The improvement and development of modern technologies, such as computerized control, automated mushroom harvesting, preparation of compost, production of mushrooms in a non-composted substrate, and new methods of substrate sterilization and spawn preparation, will increase the productivity of mushroom culture. All these aspects are crucial for the production of mushrooms with better flavor, appearance, texture, nutritional qualities, and medicinal properties at low cost. Mushroom culture is a biotechnological process that recycles ligninocellulosic wastes, since mushrooms are food for human consumption and the spent substrate can be used in different ways.
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Introduction
Mushrooms have been eaten and appreciated for their flavor, economic and ecological values, and medicinal properties for many years. They have a chemical composition which is attractive from the nutritional point of view. In general, mushrooms contain 90% water and 10% dry matter. The protein content varies between 27% and 48%, carbohydrates are less than 60%, and lipids 2–8% (Crisan and Sands 1978; Ranzani and Sturion 1998; Morais et al. 2000). The total energetic value of mushroom caps is 1.05–1.50 J/kg of fresh mushroom (Oliver and Delmas 1987; Laborde 1995). There are at least 12,000 species of fungi that can be considered to be mushrooms, with at least 2,000 species showing various degrees of edibility (Chang 1999). Furthermore, over 200 species have been collected from the wild and used for various traditional medical purposes, mostly in the Far East. About 35 mushroom species have been cultivated commercially, and of these, around 20 are cultivated on an industrial scale. The most cultivated mushroom worldwide is Agaricus bisporus (button mushroom) followed by Lentinus edodes (shiitake), Pleurotus spp (oyster mushrooms), Auricula auricula (wood ear mushroom), Flamulina velutipes (winter mushroom), and Volvariella volvacea (straw mushroom; Chang 1999). L. edodes was first cultivated in China between 1000 AD and 1100 AD, Agaricus bisporus in France in ca. 1600, and P. ostreatus in the USA in 1900. Techniques for the culture of the other less popular mushrooms were developed in China between 600 AD and 1800. However, it is only over the past two to three decades that there has been major development in basic research and practical knowledge for the creation of a significant worldwide industry (Chang and Miles 1989). Mushrooms have the ability to degrade ligninocellulosic substrates and can be produced on natural materials from agriculture, woodland, animal husbandry, and manufacturing industries (Rinker 2002), which are often landfilled or burned in the field at great cost to the environment (Anoliefo et al. 1999). However, mushroom production generates an enormous amount of used “spent” substrate, which might also be a source of environmental contamination. Currently, several uses for spent substrate are being evaluated and some of them have already been established (Rinker 2002).
Cultivation of mushrooms
Mushroom culture involves several different operations, each of which must be carefully performed. The first stage is to obtain a pure mycelium of the specific mushroom strain. The mycelium can be obtained from spores, from a piece of the specific mushroom, or from several germplasm providers (e.g., American Type Culture Collection, National Center for Agricultural Utilization Research, etc.). To obtain inoculum, the mycelium is developed on cereal grain, e.g., wheat, rye or millet, which is usually called the spawn (Chang and Hayes 1978; Chang and Miles 1989). Once developed, it is readily purchased from several mushroom companies (e.g., Sylvan, Amycel, J.B. Swayne, etc.). The purpose of the mycelium-coated grain is to rapidly colonize the specific bulk-growth substrate. The success of mushroom production depends in great part on the quality of the spawn, which must be prepared under sterile conditions to diminish contamination of the substrate. Several studies have been done to improve and develop new techniques for the production of spawn (Chu and Wang 1977; Claxton 1979; Sarkar and Chakravarty 1982; Bisht and Harsh 1984; Abdullah et al. 1995; Abosriwil and Clancy 1999; Holtz and McCulloch 1999; Friel and McLoughlin 2000; Muthukrishnan et al. 2000; http://www.sylvaninc.com/randd.html). Poppe (2000) reported that there are about 200 kinds of waste in which edible mushrooms can be produced. Substrate preparation, inoculation, incubation, and production conditions depend on the mushroom species to be cultivated (Figs. 1, 2).
Studies on the development of A. bisporus have improved its cultivation (Raper 1985; Callac et al. 1993; Stoop and Mooibroek 1999; Kothe 2001). The substrate for culturing A. bisporus is the most complex culture medium used for edible mushroom production. The compost is prepared by a two-stage process. In the first stage, a mixture of raw materials, animal manure (such as stable bedding or poultry manure), and gypsum are assembled and wetted and then formed into a stack (windrow). Water addition is controlled and the stack is dissembled and reformed at intervals. In the second stage, pasteurization is done to prepare the compost for a selective growth medium (Sinden and Heuser 1953; Wuest 1977; Fermor and Grant 1985; Overtjins 1998) on which A. bisporus will be inoculated. This two-phase process for substrate preparation has some disadvantages, e.g., more time and space are necessary for culturing. Due to this, studies have been undertaken to produce A. bisporus on a non-composted substrate in order to reduce the time and cost of mushroom culture (Murphy 1972; Sánchez et al. 2002).
L. edodes (shiitake mushroom) was traditionally grown on wood logs (Chang and Hayes 1978; Chang and Miles 1989). This method has been replaced by artificial log cultivation, which utilizes heat-treated supplemented substrates (based on sawdust) enclosed in plastic bags (bag-log cultivation). The main advantages of this method are the short time to complete a crop cycle and the higher yields (Royse 1997a). The strain, substrate composition, and length of incubation are important parameters for shiitake production on synthetic substrates used in bag-log cultivation (Zadrazil 1993; Kalberer 1995; Royse and Bahler 1986).
Pleurotus spp (oyster mushrooms) are usually grown on a wide range of ligninocellulosic materials (Poppe 2000). The materials are generally not composted prior to mushroom inoculation. The materials for growth are pasteurized to diminish contamination and increase selectivity for the oyster mushroom. The culture of Pleurotus spp is often carried out in plastic bags containing substrate inoculated with mycelium (Chang and Hayes 1978; Chang and Miles 1989). The strain used is of particular importance, since some workers develop an allergy that is identical to mushroom-workers lung and is associated with personal exposure to Pleurotus spp spores (Laborde 1995; Mori et al. 1998; Saikai et al. 2002; Senti et al. 2000). However, similar symptoms have also been observed with L. edodes spores (Laborde 1995; Senti et al. 2000). This problem has increased interest in the development of sporeless mutants for breeding sporeless strains (Laborde 1995; Obatake et al. 2003).
Recently, mushroom culture has moved toward diversification. The culture of the following has been reported: Agaricus species (e.g., A. bitorquis, A. blazei; Dhar and Gupta 1998; Kaiben et al. 1998), several Pleurotus species (e.g., P. pulmonarius, P. eryngii; Philippoussis et al. 2001), Volvariella volvacea (paddy straw mushroom; Ma and Buswell 1998; Philippoussis et al. 2001), Grifola frondosa (maitake; Lee 1994; Kirchhoff 1996; Royse 1997b; Stamets 2000), Chantarella cibarius (golden chanterelle; Danell and Camacho 1997), Morchella esculenta (yellow morel; Ower 1982; Douxi and Yue 1998), Ganoderma lucidum (Chen 1998), Auricularia polytricha (mu-erh; Silverio and Vilela 1982; Pegler 2001; Bis’ko et al. 1995), Tremella fuciformis (silver ears; Pegler 2001), and F. velutipes (honey mushroom; Psurtseva 1987). Perhaps in the near future, it might be possible to cultivate at large scale species such as Boletus reticulatus (boletes; Yamanaka et al. 2000), Hustilago maydis (huitlacoche; Pataky 2002), Tricholoma matsutake (matsutake; Vaario et al. 2002), and Tuber melanosporium (black truffle; Olivier 2000), which are very much appreciated gastronomically.
Development of technology and selection of strains to increase productivity
To increase productivity in mushroom culture, it is necessary to develop and improve the control and computerized monitoring of growing rooms, automated mushroom-harvesting machines, hydroblending and pre-wet equipment (heap turners), or to develop methods for producing mushrooms on a non-composted substrate and new techniques for sterilization, etc. (Hawton et al. 2000).
A computerized environmental control system is an invaluable tool for mushroom culture. The computer monitors environmental parameters, such as temperature, humidity, airflow, pressure, carbon dioxide, and oxygen content. However, automatic control of ammonia levels and moisture in the casing soil is still not widely applied. About two decades ago, the first climate computers were introduced to Dutch mushroom-growing and now are widely used in the industry (Lamber 2000). Climate control in production plants allows the monitoring and control of several mushroom production rooms with minimum human input. The computerized environmental control system allows the grower to inspect and adjust the environmental conditions of the plant by using remote access (modem) capabilities (Walker 1996). There are several companies which provide environmental control systems (e.g., DuraFlex, Jaybird Manufacturing, Agricultural Engineering, etc.).
Picking and packing constitute the most expensive part of the overall production process. In the past 15 years, several studies have been carried out to develop automated mushroom-harvesting machines. Some companies offer automated harvesting systems, which range from small, modular semiautomatic picking aids to fully automated, robotic systems designed for line-picking (Kensal Automation; Astell 1996). The harvesting operation includes mushroom location, sizing, selection, and picking. The mechanical properties used for the analysis of automated harvesting were obtained from compression experiments with cylindrical mushroom sample-pieces (Hiller 1994). Reed et al. (1995) evaluated the automated harvesting of Agaricus bisporus by machine at the laboratory level; and the resulting pilot harvester was successfully tested on a commercial mushroom farm. The apparatus combines several handling systems and mechatronic technologies. Mushrooms are located and sized using image analysis and a monochromatic vision system. An expert selection algorithm then decides the order in which they should be picked and what picking action (bend, twist, or both) should be used (Tillett and Batchelor 1991; Reed et al. 1997). One of a pair of suction cup mechanisms attached to the single head of a Cartesian robot is then deployed, which can delicately detach individual mushrooms and place them gently into a specially designed, compliant finger conveyer. After high-speed trimming, a gripper mechanism is finally used to remove mushrooms from the conveyor into packs at the side of the machine (Reed et al. 1995, 2001).
The pre-wet heap machine was designed to achieve a quick homogeneous mix of water and the raw materials used in phase 1 of the culture of A. bisporus, to improve the efficiency of the composting process by reducing the amount of time required to achieve the same or better quality compost. Some benefits of using the pre-wet compost turners include improving compost quality, homogenous blending of up to 200 t/h, better odor control, less water run-off, raw material savings, reducing of phase 1 time by over 50%, reducing operating and capital costs, and increasing production yields, crop uniformity, and profit potential. The design of new equipment to improve productivity is continuously in development. Recently, a new tunnel/bunker filling system has been developed, which consists of filling the bunkers or tunnels using overhead layering techniques, but only from one end of the bunker/tunnel and not through holes in the tunnel roof, with the use of overhead and out-of-sight conveyors/elevators (Traymater Machinery).
New methods to produce and increase the productivity of a wide variety of exotic mushrooms have been developed. The Mycocell system (Mycocell Technologies, UK) is a method based on microwave sterilization of pre-packaged substrate to which the spawn, nutrients, and other supplements can be added. In this case, radiation used in the treatment of the substrates changes the cellulose and increases ease of breakdown by the mycelium. Several nutrients can be added and mixed thoroughly, there are no risks of substrate contamination, and colonization of the substrate by the mycelium considerably increases. The commercial benefits of this production system include lower cost, low energy requirements, automation, low labor demand, lack of down-time, light and cheap transport, low contamination risk, and long shelf-life. The Mycocell system allows the successful culture of exotic mushrooms such as L. edodes, P. ostreatus, P. pulmonarius, P. eryngii, P. djamor, P. cystidiosus, Pholiota sp., Hypsizygus sp., F. velutipes, Agrocybe aegerita, G. lucidum, Psilocybe sp., Grifola frondosa, Hericium sp., and Auricularia (Hawton et al. 2000).
A technology called variable frequency speed control for alternating current motors (Keljik 1995) may be useful for mushroom farms and could benefit the industry by improved control of air velocity in the growing environment, resulting in lower electricity consumption (Lomax 1989, 1992).
The strain used in the culture is crucial for success in mushroom production and marketing. A strain with a high ability to invade the substrate and to fruit diminishes the time of incubation and enhances productivity. The consistency and texture of the mushroom are crucial to diminish losses during packing. The first Agaricus bisporus hybrid was obtained by breeding about 20 years ago. However, most of the strains currently used are similar to the first hybrid obtained (Sonnenberg 2000; Kerrigan 2000). The increase in mushroom production has mainly been the result of increasing the cultivation area, improving production techniques, and compost preparation rather than the development of new highly productive strains. Unfortunately, most information about the use of genetics in basidiomycete growing and breeding has come from the study of less economically important species, such as Schizophyllum commune and Coprinus cinereus. However, the findings in these organisms have been adapted and some progress has been made with economically important mushrooms, such as A. bisporus and Pleurotus ostreatus (Kothe 2001). The use of DNA-based technology has accelerated breeding activities and will help the mushroom-breeding programs (Stoop and Mooibroek 1999). An important advance in developing techniques for breeding is based on the development and detection of genetic markers (Sonnenberg 2000). Research on the molecular basis of mating-type genes has been very important for the development of strains with high yields and resistance to bacterial diseases (Oliver and Delmas 1987), viral diseases (Harmsen et al. 1991; Sonnenberg et al. 1995), and fungal diseases (Dragt et al. 1995; Kerrigan 2000).
Additional benefits of mushroom culture
Spent mushroom substrate has been used as animal feed, since its degradation by the mushroom can improve its nutritional quality (Jalc et al. 1996a, 1996b; Adamovic et al. 1998; Díaz-Godínez and Sánchez 2002) and digestibility by the ruminant (Zadrazil 1977, 1996, 1997, 1998, 2000; Domsch and Zadrazil 1982; Capelari and Zadrazil 1997; Braun et al 2000; Díaz-Godínez and Sánchez 2002). Díaz-Godínez and Sánchez (2002) found that when maize straw generated after mushroom cultivation was added to the diets of sheep, the weight gain of the sheep increased, as did the efficiency of the straw feed conversion.
After mushroom cultivation, the spent substrate is still very valuable. Several studies have reported the use of spent mushroom straw for mushroom re-cultivation. For example, it has been suggested that spent mushroom compost enriched with cotton seed meal and soya meal can be used for Agaricus cultivation, spent Pleurotus substrate for King Stropharia cultivation (Poppe 1995) and spent Agaricus compost with added cotton waste for Volvariella production (Oei 1991). Chang and Miles (1989) studied the use of spent Volvariella substrate for the production of P. sajor-caju. The use of spent straw generated after the cultivation of Ganoderma lucidum and F. velutipes has also been recommended for the production of other mushrooms, such as A. bisporus or C. comatus (Xiao 1998). A. bisporus spent substrate can be used for the cultivation of Volvariella (Poppe 2000). Spent mushroom substrate can also be used as casing material for the production of Agaricus (Nair and Brandley 1981; Shandilya 1989; Singh et al. 1992, 2000).
Spent mushroom substrate is also a beneficial product for the enrichment of soils, restoring areas that have been destroyed through development, deforestation or environmental contamination. Some studies have been done on the use of spent mushroom substrate in vegetable and flower greenhouses (Lohr et al. 1984; Verdonck 1984; Steffen et al. 1994, 1995; Szmidt 1994; Söchting and Grabbe 1995; Celikel and Tuncay 1999), in field vegetable and fruit crops (Male 1981; Delver and Wertheim 1988; Pill et al. 1993; Ranganathan and Selvaseelan 1997; Stewart et al. 1998; AntSaoir et al. 2000; Batista et al. 2000), in nursery and landscape gardening (Chong and Wickware 1989; Chong and Rinker 1994; Chong 1999), and in soil amendment (Wuest and Fahy 1991; Stewart et al. 2000). Currently, there are some industries that manufacture and sell different kinds of compost based on spent mushroom substrate (http://www.nutrasoils.com, http://www.southmill.com, http://www.americanmushroom.org, http://www.laurelvalleysoils.com).
The potential of spent mushroom substrate to degrade organopollutants and its importance in the environmental bioremediation have been reported (Kuo and Regan 1998; Eggen 1999; Semple et al. 2001; Webb 2001; Lau et al 2003; Law et al. 2003; Xawek et al. 2003).
Conclusions
Edible mushrooms have been cultivated for many years and it is expected that their production will increase further in the future, due to market demand. The improvement and development of modern technologies, such as computerized control systems to control environmental parameters, automated harvesting, techniques for the production of mushrooms in a non-composted substrate, and new methods for substrate sterilization and spawn preparation, will increase the productivity of mushroom culture. The development of techniques to produce mushrooms in a non-composted substrate will make the cropping cycle of the mushroom shorter, diminish the cost of the process, and minimize the odor generated during the composting process, which is a problem of environmental contamination. The breeding of new strains will improve the development of strains with high yield and resistance to diseases, increase productivity, and diminish the use of chemicals for pest control. All these aspects will be crucial in the production of mushrooms with better flavor, appearance, texture, nutritional qualities, and medicinal properties at low cost. Perhaps in the near future, large-scale cultivation might be possible for species which are gastronomically very much appreciated, such as B. reticulatus, Tricholoma matsutake, Tuber melanosporium, and Hustilago maydis.
The production of mushrooms generates a large amount of spent substrate, which can be used as animal feed, soil conditioner, for mushroom recultivation, and for bioremediation, among other applications. Mushroom culture is a biotechnological process that recycles ligninocellulosic wastes, since these are converted to a food for human consumption and the spent mushroom substrate can be used in several ways.
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I am grateful to Dr. A.L. Demain for critical reading of the manuscript.
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Sánchez, C. Modern aspects of mushroom culture technology. Appl Microbiol Biotechnol 64, 756–762 (2004). https://doi.org/10.1007/s00253-004-1569-7
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DOI: https://doi.org/10.1007/s00253-004-1569-7