Fungal Diversity https://doi.org/10.1007/s13225-019-00422-9 (0123456789().,-volV)(0123456789().,- volV) REVIEW Fungicolous fungi: terminology, diversity, distribution, evolution, and species checklist 1,2 1,7 3 4 5 Jing-Zu Sun • Xing-Zhong Liu • Eric H. C. McKenzie • Rajesh Jeewon • Jian-Kui (Jack) Liu • 1 6 2 Xiao-Ling Zhang • Qi Zhao • Kevin D. Hyde Received: 20 September 2018 / Accepted: 4 March 2019 Ó School of Science 2019 Abstract Fungicolous fungi are a very large, diverse, ecological and trophic group of organisms that are associated with other fungi. This association occurs with species of different lineages across the fungal kingdom. They are recognized as symbionts, mycoparasites, saprotrophs, and even neutrals. Wherever fungi have been found, fungicolous taxa have also been found. Homogeneous environments favour the development of highly adapted and coevolved fungicolous species, which could have led to host-specificity aspects. As a primary consumer, fungicolous fungi decrease the turnaround time of certain nutrients in food webs, due to their special often-rapid life cycles. They may also significantly affect population dynamics and population sizes of their hosts in aquatic or terrestrial ecosystems. As mycoparasites of pathogenic fungi, some fungicolous fungi have been explored as biocontrol agents. They may also cause serious diseases of cultivated edible and medicinal mushrooms, decreasing both yield and quality. Fungicolous fungi could be used as model organisms that may help determine better understanding of species interactions, fungal evolution and divergence, and fungicolous mechanisms. This review summarizes our current understanding of fungicolous fungi, with a particular focus on the terminology, diversity, global distribution, and interaction with their hosts. We also provide a checklist including 1552 fungicolous fungal taxa so far recorded following the updated classification schemes. There is a need for further investigations on this ecologically important group of fungi to better understand their biology, ecological aspects, origin and divergence, host- specificity and application in biocontrol. Accurate identification of these fungi as pathogens and their significance in quarantine purposes on the mushroom industry need further evaluations so that efficient control measures can be developed for better disease management purposes. Keywords Biocontrol Á Host-specificity Á Mushroom diseases Á Mycoparasites Á Species diversity & Xing-Zhong Liu 4 Department of Health Sciences, Faculty of Science, [email protected] University of Mauritius, Reduit, Mauritius & Kevin D. Hyde 5 Center for Bioinformatics, School of Life Science and [email protected] Technology, University of Electronic Science and Technology of China, Chengdu 611731, People’s Republic of 1 State Key Laboratory of Mycology, Institute of China Microbiology, Chinese Academy of Sciences, No. 3 Park 1, 6 Key Laboratory for Plant Diversity and Biogeography of East Beichen West Road, Chaoyang District, Beijing 100101, Asia, Kunming Institute of Botany, Chinese Academy of People’s Republic of China Science, Kunming 650201, People’s Republic of China 2 Center of Excellence in Fungal Research, Mae Fah Luang 7 Department of Microbiology, College of Life Science, University, Chiang Rai 57100, Thailand Nankai University, Jinnan District, Tianjin 300350, People’s 3 Manaaki Whenua Landcare Research, Republic of China Private Bag 92170, Auckland, New Zealand 123 Fungal Diversity Introduction consequently studies led to the discovery of asexual-sexual morph connections of fungicolous fungi in the Hypocre- Fungi as symbionts are found associated with every major ales, and mycoparasitic Heterobasidiomycetes (Reid 1990; group of prokaryotes and eukaryotes: bacteria, algae, ani- Helfer 1991;Po˜ldmaa and Samuels 1999). Apparently, mals, insects, and plants (Blackwell 2011; Liu et al. 2010; most surveys mainly focused on fungicolous fungi asso- Swe et al. 2008a, b, 2011; Wijayawardene et al. ciated with fruiting bodies of mushrooms (Rogerson and 2017a, b, 2018a, b). Some fungi consistently associated Samuels 1989, 1993, 1994). Gams et al. (2004) reported with other fungi are named as fungicolous (or mycophilic) that there were 1700 fungicolous taxa (including sexual fungi (Barnett 1963; Rudakov 1978). Fungicolous fungi and asexual morphs, and fungus-like oomycetes). have evolved across different lineages within the fungal Wijayawardene et al. (2017a, b) listed 55 genera of kingdom (Deighton 1969; Poinar and Buckley 2007; Ascomycota having potential fungicolous features. Ober- Po˜ldmaa 2011; Pintye et al. 2015; Melo et al. 2016; Powell winkler (2017) reviewed yeast-form fungicolous fungi in et al. 2017). These taxa survive alongside their hosts Pucciniomycotina. Recently microbiome analyses revealed (Fig. 1), which co-occur in aquatic or terrestrial ecosys- that diversity of fungicolous species associated with fungal tems from temperate and tropical to arctic regions fruiting bodies are much more than expected (Leonardi (Deighton 1969; Freeman et al. 2009; Opik et al. 2010; et al. 2018). Po˜ldmaa 2011; Pintye et al. 2015). As one of the primary Fungicolous fungi could kill their hosts via antagonistic consumers, fungicolous fungi decrease the turnaround time involving the secretion of enzymes or antibiotics, or of certain nutrients in food webs, due to their special living competition of nutrition and niche (Kubicek et al. 2011; strategy and have often rapid life cycles (Marano et al. Chaverri and Samuels 2013; Karlsson et al. 2015). The 2011; Hargreaves et al. 2018). They may significantly aggressive fungicolous taxa, such as Gliocladium spp. and affect population dynamics and population sizes of their Trichoderma spp., have been explored as biological hosts in aquatic or terrestrial ecosystems (Marano et al. fungicides (Rosenheim et al. 1995). Ampelomyces quis- 2011; Parratt and Laine 2018). Most of the fungicolous qualis, a cosmopolitan host-specific mycoparasite of Ery- species are mycoparasites or hyperparasites (Barnett 1963; siphales, has been explored as a biocontrol agent to Boosalis 1964; Bartkowska 2007; Baiswar et al. 2014) and suppress powdery mildew disease (Sundheim 1982; Sio- can cause devastating diseases of mushroom in nature and zios et al. 2015). Sphaerellopsis filum (Eudarluca caricis), industry by reducing the yield and quality worldwide a host-specific mycoparasite of Puccinia, has been applied (Foulongne-Oriol et al. 2011; Sun et al. 2016a; Kim et al. to suppress plant rust disease (Pei and Yuan 2005; Black 2017). On the other hand, they are also important in sup- 2012). The secondary metabolites from fungicolous fungi pressing fungal diseases of plants and act as potential are considered as potential candidates for exploring anti- biocontrol agents (Bartkowska 2007; Baiswar et al. 2014; fungal drugs (Lorito et al. 1994; Mudur et al. 2006; Sun Videira et al. 2015). et al. 2016b; Junker et al. 2018). Gliotoxin and gliovirin Studies on fungicolous fungi can be traced back to two produced by Trichoderma virens have received much centuries ago (Nees von Esenbeck 1817; Fries and Nord- attention for their role in biocontrol of soil-borne fungal holm 1817; Willdenow et al. 1833) and their mycoparasitic pathogens (Mukherjee et al. 2013). More than 50 com- activity on mushrooms in the field was observed in the mercial biocontrol agents based on these fungicolous taxa 1760s (Gray and Morganjones 1981). Cladobotryum and their secondary metabolites have been successfully agaricina was the first fungicolous ascomycete on Agari- developed to suppress plant fungal pathogens (Black 2012; cus sp. and Asterophora agaricoides was the first fungi- Karlsson et al. 2015). colous basidiomycete on the fruiting body of an Agaricus Previous studies have made considerable progress on the species (Fries and Nordholm 1817). The zygomyceteous diversity, ecology, taxonomy, and application of fungi- Mucor fusiger was found to infect some species of Agar- colous fungi (Barnett 1963; Barnett 1964; Curtis et al. icales (Willdenow et al. 1833). Consequently, many more 1978; Gupta and Mukerji 2010;Po˜ldmaa 2011; Atanasova diverse species of fungicolous fungi associated with dif- et al. 2013; Kosawang et al. 2014; Karlsson et al. 2015; ferent taxonomic lineages were reported (Tubaki 1955; Siozios et al. 2015; Powell et al. 2017). However, the Nicot 1967; Hashioka and Nakai 1980; Rogerson and diversity of fungi are possibly still underestimated due to Samuels 1989, 1993, 1994; Gupta and Mukerji 2010; inherent problems associated with culture-independent Po˜ldmaa 2011; Ellenberger et al. 2014; Pintye et al. 2015). DNA sequencing methods (Hoppe et al. 2016; Carini et al. The diversity of fungicolous fungi was extensively 2017; Leonardi et al. 2018), species concepts, classifica- investigated during the 1960s and 1970s (Barnett 1963; tion, asexual- and sexual morph connections, and nomen- Barnett 1964; Curtis et al. 1978; De Hoog 1978), and clatural compliance to the ‘one fungus one name’ principle (Rossman et al. 2013; De Beer et al. 2016). 123 Fungal Diversity Fig. 1 Fungicolous fungi associated with host fungi. a Hypomyces boletuphus on Boletaceae sp., b Asterophora agaricoides on Agaricus sp., c Hypomyces boletus on Boletus sp., d Hypomyces mycophilus on Agaricomycetes e Lecanicillium fungicola var. aleophilum on Agaricus bisporus, f Hypomyces rosellus on Agaricus bisporus, g Mycogone perniciosa on Agaricus bisporus, h Hypomyces sp. on Polyporaceae, i Fusarium solani on Tuber sp., j Diploospora