Occurrence and function of enzymes for lignocellulose degradation in commercial Agaricus bisporus cultivation

Appl Microbiol Biotechnol (2017) 101:4363–4369 DOI 10.1007/s00253-017-8294-5 MINI-REVIEW Occurrence and function of enzymes for lignocellulose degradation in commercial Agaricus bisporus cultivation Mirjam A. Kabel 1 2 & Edita Jurak & Miia R. Mäkelä 3,4 & Ronald P. de Vries 3 Received: 5 February 2017 / Revised: 6 April 2017 / Accepted: 8 April 2017 / Published online: 2 May 2017 # The Author(s) 2017. This article is an open access publication Abstract The white button mushroom Agaricus bisporus is economically the most important commercially produced edible fungus. It is grown on carbon- and nitrogen-rich substrates, such as composted cereal straw and animal manure. The commercial mushroom production process is usually performed in buildings or tunnels under highly controlled environmental conditions. In nature, the basidiomycete A. bisporus has a significant impact on the carbon cycle in terrestrial ecosystems as a saprotrophic decayer of leaf litter. In this mini-review, the fate of the compost plant cell wall structures, xylan, cellulose and lignin, is discussed. A comparison is made from the structural changes observed to the occurrence and function of enzymes for lignocellulose degradation present, with a special focus on the extracellular enzymes produced by A. bisporus. In addition, recent advancements in whole genome level molecular studies in various growth stages of A. bisporus in compost are reviewed. Keywords Agaricus bisporus . Xylan structure . Lignin . Genome . Enzymes * Ronald P. de Vries 1 Laboratory of Food Chemistry, Wageningen University, Bornse Weilanden 9, 6708 WG Wageningen, The Netherlands 2 Department of Biotechnology and Chemical Technology, Aalto University, Kemistintie 1, 02150 Espoo, Finland 3 Fungal Physiology, Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands 4 Division of Microbiology and Biotechnology, Department of Food and Environmental Sciences, University of Helsinki, Viikinkaari 9, Helsinki, Finland Introduction Edible mushrooms are an important agricultural product worldwide. Only few of these edible mushrooms, however, can be cultivated with the most extensively cultivated species being Agaricus bisporus (30–40%), Pleurotus ostreatus (25– 27%), Lentinula edodes (17%) or Volvariella volvacea (16%) (Chang 1999; ISMS Edible mushrooms 2017; Royse 2014). The white button mushroom A. bisporus can be grown on various raw materials, such as composted cereal straw and animal manure. This cultivation process is usually conducted in buildings or tunnels where the environmental conditions, such as temperature, humidity and concentration of carbon dioxide, are controlled. The major regions of A. bisporus cultivation are Europe, North America, China and Australasia. Besides its commercial importance, the basidiomycete A. bisporus has a natural life style as a saprotrophic leaf litter (non-wood)-inhabiting decayer of plant biomass and, hence, contributes to the carbon cycle in terrestrial ecosystems (Morin et al. 2012). It has a widespread geographical distribution in natural habitats such as arid places or forests in NorthAmerica and forests or coastal dunes in Europe or Africa (Geml et al. 2008; Kerrigan 1995; Callac et al. 2002). The life cycle of A. bisporus consists of a vegetative mycelial phase with a subsequent reproductive phase in which fruiting bodies are formed. Vegetative mycelium, generally, supplies nutrients for the growth of fruiting bodies, while the role of fruiting bodies is reproduction (Bonner et al. 1956). The role of enzymes secreted by A. bisporus during either vegetative or reproductive phases has received a steady interest (Fig. 1) but has not been reviewed so far. In this mini-review, the occurrence and function of enzymes for lignocellulose degradation reported for commercial mushroom cultivation are discussed, focussing in particular on the extracellular enzymes of A. bisporus. Enzyme activity 4364 Appl Microbiol Biotechnol (2017) 101:4363–4369 Fig. 1 Scientific publications (Web of Science) per year of the topic Agaricus bisporus or Agaricus bisporus and enzyme and protein occurrence are compared with recent published advancements in understanding the genetic potential of A. bisporus and the gene expression in both vegetative and reproductive phases. A correlation between the produced enzymes and the fate of lignocellulose structures during A. bisporus growth is also presented. We conclude with an outlook on how the scientific insights provided in this minireview can help to improve commercial cultivation of mushrooms. Commercial cultivation of Agaricus bisporus The production of compost in commercial production facilities comprises the bioconversion of raw materials into a substrate supporting the growth of A. bisporus. The whole process, from composting to fungal mycelium growth and production of fruiting bodies, has been optimized over the last century. A schematic overview of the process is shown in Fig. 2. Process optimization was based on empirical approaches, while a full understanding of the degradation and conversion pathways at the various conditions performed was not considered. Now, the mushroom industry more and more believes that the next improvements in their process will result from a more detailed understanding of the biological mechanisms and metabolic pathways involved in the production process. Hence, the traditional craft of mushroom production for food, from agricultural by-products and manure, becomes a true science. World-wide, the type of raw materials used to produce a good substrate for A. bisporus growth varies, although they always contribute as a carbon and a nitrogen source (Iiyama et al. 1994). In Europe, the A. bisporus substrate or compost is produced from a mixture of wheat straw (40 to 50% of the total dry weight), horse manure or stable bedding (20–25%), poultry manure (10–15%) and gypsum (5 to 10%). Horse manure or stable bedding is only used in certain countries where these ingredients are available in significant amounts. The production of the A. bisporus substrate is usually performed in two indoor phases (Fig. 2): Phase I (PI) and Phase II (PII). At the start of PI, raw materials are mixed and, typically, mesophilic microbiota starts to develop. This microbiota converts part of the carbohydrates and proteins into heat and ammonia. As the temperature rises, the mesophilic microbiota is naturally replaced by thermophilic microbiota (Gerrits 1988). In PI, the compost temperature rises up to 80 °C and could last 3 to 7 days. These reactions cause the wheat straw to soften. During PII, the compost is conditioned (8 h at 56 °C), partly by blowing air and partly by further growth of microbiota, and kept at 45 °C until the process air is virtually free of ammonia (Gerrits 1988). In this phase, microorganisms, in particular actinomycetes and fungi, are reported to g (...truncated)