Mushroom cultivation in the circular economy

Applied Microbiology and Biotechnology https://doi.org/10.1007/s00253-018-9226-8 MINI-REVIEW Mushroom cultivation in the circular economy Daniel Grimm 1 & Han A. B. Wösten 1 Received: 28 May 2018 / Revised: 4 July 2018 / Accepted: 4 July 2018 # The Author(s) 2018 Abstract Commercial mushrooms are produced on lignocellulose such as straw, saw dust, and wood chips. As such, mushroom-forming fungi convert low-quality waste streams into high-quality food. Spent mushroom substrate (SMS) is usually considered a waste product. This review discusses the applications of SMS to promote the transition to a circular economy. SMS can be used as compost, as a substrate for other mushroom-forming fungi, as animal feed, to promote health of animals, and to produce packaging and construction materials, biofuels, and enzymes. This range of applications can make agricultural production more sustainable and efficient, especially if the CO2 emission and heat from mushroom cultivation can be used to promote plant growth in greenhouses. Keywords Mushroom . Edible mushroom . Fungus . Spent mushroom substrate . Circular economy . Mycelium material Introduction The transition to a circular economy has shifted from a vision (Boulding 1966) to actual policy making. In this view, agricultural waste streams are no longer considered a debit entry but are considered valuable resources. The 0.25 billion tons of straw that were burned in China alone in 2009 (Feng et al. 2011) could have been used in a wide variety of applications. For instance, lignocellulosic waste streams can be converted into second-generation biofuels. As such, it can contribute to the aim of the European Union to have 10% of the transport fuel originating from renewable sources by 2020 (www.ec. europa.eu/energy/en/topics/renewable-energy). Although use of resources for production of second-generation biofuels does not compete with food, this may not be the most circular application. Growing mushroom-forming fungi on these substrates may prove more sustainable. This would not only result in edible and/or medicinal mushrooms but also in spent mushroom substrate (SMS) that can be used for a wide variety of applications. Mushrooms represented a market of 63 billion US dollars in 2013 (Royse et al. 2017). This market represents medicinal mushrooms (38%) and wild (8%) and cultivated edible (54%) * Han A. B. Wösten 1 Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584, CH Utrecht, The Netherlands mushrooms. At a global scale, consumption of mushrooms has increased from 1 to 4.7 kg of cultivated edible mushrooms per capita in the period 1997 to 2013 (Royse et al. 2017). Consumption is expected to further increase in the next years resulting in a sales going from 34 to 60 billion US dollar annually (see e.g., https://www.zionmarketresearch.com/ news/global-mushroom-market). In 2013, China produced 87% of the 35 billion kg of cultivated edible mushrooms, most of which being consumed in this country. This explains why the button mushroom (Agaricus bisporus and relatives), the most popular edible mushroom in the Western world, is only at the fourth position of most cultivated mushrooms. The top three consists of Lentinula (shiitake and relatives), Pleurotus (oyster mushrooms), and Auricularia (wood ear mushrooms). Edible mushrooms are considered nutritious foods. They contain 5–15% dry matter, have a balanced composition of minerals and vitamins, and are rich in fiber and protein (± 2% fresh weight) (Mattila et al. 2002). Their amino acid composition is better when compared to that of vegetables like potatoes and carrots. Moreover, mushrooms are low in calories (27–30 kcal/100 g) with a low amount of fat (1.3–8% of dry weight mushrooms) and digestible carbohydrate (Mattila et al. 2002). SMS is available in huge amounts underlined by the fact that 1 kg of fresh mushrooms results in 5 kg of spent substrate (i.e., 2 kg dry weight) (Finney et al. 2009). SMS was long considered a waste stream. Yet, it can be used for production to produce high-quality compost (Uzun 2004; Polat et al. 2009) or other mushrooms (Stamets 1993), to feed animals Appl Microbiol Biotechnol and to improve their health (Song et al. 2007; Nasehi et al. 2017), to make biofuel production more effectively (Phan and Sabaratnam 2012), to produce materials (Jones et al. 2017; Islam et al. 2017; Appels et al. 2018), and to extract enzymes for industries and bioremediation (Phan and Sabaratnam 2012). In this review, we will discuss production of mushrooms and the potential applications of SMS in a circular economy. We will not discuss the use in bioremediation. For this, we refer to, for instance, Frutos et al. (2016); Siracusa et al. (2017); and Mir-Tutusaus et al. (2018). Mushroom production Cultivated edible mushrooms are the fruiting bodies of basidiomycetes with a saprobic life style. These basidiomycetes can be divided into primary, secondary, and tertiary decomposers (Rahi et al. 2009). Primary decomposers such as the oyster mushrooms (Pleurotus spp.) and shiitake (Lentinula edodes) degrade (hemi)cellulose, lignin, and other components of plant material. Unlike secondary and tertiary decomposers, they do not depend on other organisms and their metabolites. Secondary decomposers such as the button mushroom typically colonize composted materials, while tertiary decomposers such as Agrocybe spp. are generally found in soils. The three categories of decomposers represent a continuum in the metabolic transition from lignocellulosic and other organic materials to soil. Indeed, it is possible to completely compost agricultural waste through the successive cultivation of mushrooms from different stages in this continuum (Stamets 1993). This, however, is hardly, if at all, applied in large-scale mushroom production. Many mushroom-forming fungi belonging to the class of primary decomposers can be cultivated on a range of lignocellulosic material (Stamets 1993), including various types of straw, cotton seed hulls, corn cobs, peanut shells, cotton from textile industry, coffee pulp, paper (Sánchez 2010), and leaves (Shah et al. 2004). The oldest form of mushroom cultivation is probably the outdoor log culture, which has been used in China to cultivate shiitake at least for a millennium. Nowadays, this technique has largely been replaced with the more effective indoor cultivation on Bartificial logs,^ plastic bags filled with nutrient complemented sawdust-based substrates. Once the bag is colonized, it is unpacked to allow fruiting. The sawdust is being held together by mycelium, like glue, and will not fall apart. Very similar to the artificial logs are the column cultures that consist of long plastic bags that are hung from the ceiling. Once the mycelium has colonized these bags, holes are punched into the plastic to allow mushroom fruiting. Cultivation of Pleurotus ostreatus results in about 50% carbon dioxide, 20% water, 10% mushrooms, and 20% resid (...truncated)