A lichenicolous fungus is a member of a specialised group of fungi that live exclusively on lichens as their host organisms. These fungi, comprising over 2,000 known species across 280 genera, exhibit a wide range of ecological strategies, including parasitism, commensalism, and mutualism. They can be found in diverse environments worldwide, from tropical to polar regions, and play important roles in lichen ecology and biodiversity. Lichenicolous fungi are classified into several taxonomic groups, with the majority belonging to the Ascomycota and a smaller portion to the Basidiomycota. Their interactions with host lichens range from mild parasitism to severe pathogenicity, sometimes causing significant damage to lichen communities.
While the study of lichenicolous fungi dates back to the mid-18th century, recent decades have seen major advancements through modern research methods, including molecular techniques, metagenomics, and sophisticated imaging. These fungi show varying levels of host specificity, with some species restricted to a single lichen genus or species, while others can colonise multiple hosts. A unique subset, known as lichenicolous lichens, initiates its lifecycle as parasites but eventually becomes lichenised through a process called kleptosymbiosis. Various ecological and environmental factors, including altitude, microhabitat availability, and host specificity, influence the diversity and distribution of lichenicolous fungi.
The study of lichenicolous fungi presents unique challenges due to their microscopic size and intimate association with their hosts. Researchers employ various methods, from traditional culture techniques to advanced molecular approaches. Isolating and culturing of these fungi can be difficult, often requiring specialised media and growth conditions. Molecular methods have revolutionised the field, enabling more accurate identification and phylogenetic analysis. Nevertheless, distinguishing foreign hyphae within lichen thalli from the proper (the fungal component of the lichen) remains a challenge.
Recent research has broadened our understanding of lichenicolous fungi, particularly within groups such as black fungi and the genus Cladophialophora. These studies have not only revealed new species but also demoinstrated the potential for lichens to serve as refugia for specialised fungal organisms. Advancements in isolation techniques, culturing methods, and molecular analyses have advanced the field. The actual number of lichenicolous fungal species may be much higher than currently described, potentially reaching 3,000–5,000 species.
Definition and characteristics
Lichenicolous fungi are a specialised group of fungi that live exclusively on lichens as their host organisms. The term "lichenicolous" comes from Latin, with "lichen" referring to the host and "cola" meaning "inhabitant". These fungi are distinct from the fungal component of lichens themselves, which are known as lichenised fungi. The study of lichenicolous fungi dates back to the mid-18th century, predating the recognition of lichens as symbiotic organisms.
Lichenicolous fungi represent a highly diverse group, with over 2,000 known species across 280 genera, reflecting a wide range of ecological strategies and relationships with their lichen hosts. As of 1981, it was estimated that there might be as many as 300 genera and 1,000 species of lichenicolous fungi. These relationships vary widely, including parasitism, where the fungus harms the lichen; commensalism, where the fungus benefits without affecting the lichen; and mutualism, where both organisms benefit. Lichen thalli provide a complex and varied habitat for lichenicolous fungi, characterised by biological gradients that range from actively growing to decaying parts. This diversity within a single thallus creates a spectrum of microenvironments, which may contribute to the diversification of fungal life strategies. For example, certain lichen-associated fungi specialise in colonising or , structures lacking living host cells. Others prefer decaying parts of lichens, linking necrotic to saprobic life styles. The presence of these biological gradients within lichen thalli may act as a catalyst for the evolution and adaptation of lichenicolous fungi, potentially explaining the wide range of ecological relationships observed, from commensalism to parasitism. This complexity within the lichen habitat has led some researchers to suggest that lichens may serve as a 'cradle' for fungal evolution, fostering the development of diverse fungal life strategies. Some lichenicolous fungi are pathogenic, while others are saprotrophic, decomposing dead lichen tissues. A few lichenicolous fungi eventually become lichenised themselves, integrating into the lichen structure. Lichenicolous fungi can be non-lichenised or lichenised, obligate or facultative, and may or may not induce symptoms on the host. They are part of the complex microbiome associated with lichens, which includes bacteria, algae, and other fungi.
Lichenicolous basidiomycetes, which make up about 5% of all known lichenicolous fungi as of 2018, include both homobasidiomycetes and heterobasidiomycetes. Homobasidiomycetes typically have basidia (spore-producing structures) that lack septa (internal partitions) and non-gelatinous basidiomata (fruiting bodies), while heterobasidiomycetes have septate basidia and gelatinous basidiomata.
Morphologically, lichenicolous fungi can take diverse forms. They may produce visible fruiting bodies on the surface of the host lichen, or exist as hyphae within the host thallus. Some species can cause gall-like structures or other deformations in their hosts.
By 2018, there were 2,319 accepted species of lichenicolous fungi, including around 1,250 species of lichenicolous ascomycetes in 280 genera, and 62 species of lichenicolous basidiomycetes in ten genera. These can be categorised into three main groups:
Obligately lichenicolous species (2,000 taxa) Lichenicolous lichens (257 taxa) Facultatively lichenicolous taxa (62 taxa)
Advancements in molecular techniques and increased exploration have greatly expanded the known diversity of lichenicolous basidiomycetes, nearly doubling the species count since 2018.
Diversity and classification
The known diversity of lichenicolous fungi has increased significantly in recent decades. This growth in known diversity reflects a resurgence of interest in lichenicolous fungi in the late 20th century. For example, Clauzade and Roux compiled 457 species in 1976, which increased to 686 species by 1989. In 1997, there were 894 accepted species of obligately lichenicolous fungi. By 2018, this number had grown to over 1,800, with a rapid rate of discovery, averaging 45 new infrageneric taxa added per year over the past two decades. In total, about 1,170 infrageneric taxa have been added since 1990.
Lichenicolous basidiomycetes, a diverse group within the Basidiomycota, are primarily found in the subdivisions Agaricomycotina and Pucciniomycotina. These subdivisions encompass a wide range of fungal forms, including those that produce complex fruiting bodies and those with simpler, often parasitic forms.
Within the Agaricomycotina, lichenicolous species are present in two classes. In the Agaricomycetes, lichenicolous species are found in five of its eighteen orders: Agaricales, Atheliales, Boletales, Cantharellales, and Corticiales. In the Tremellomycetes, lichenicolous species are found in two of its five orders: Filobasidiales and Tremellales. Within the Pucciniomycotina, lichenicolous species are found in three classes: Agaricostilbomycetes, Cystobasidiomycetes, and Microbotryomycetes.
As of 2018, there were 93 known species of lichenicolous basidiomycetes (plus 7 facultatively lichenicolous taxa). Studies published since then have reported the discovery of many new species and even new genera. By 2022, the number of known species had nearly doubled to almost 200. To put this diversity in context, the estimated 300 genera and 1000 species of lichenicolous fungi (as of 1981) can be compared with the 150 genera and 700 species of Gasteromycetes, or 90 genera and 600 species of Pezizales.
The description of the new genus Crittendenia in the Pucciniomycotina represents a major taxonomic development, as it redefines the classification of several host-specific parasitic species previously placed under Chionosphaera. Another development is the recognition of several species complexes, such as Syzygospora physciacearum and Tremella parmeliarum, which have been split into multiple distinct species, often with high host specificity.
Lichenicolous species are also found among black fungi, a group characterised by dark-coloured mycelia due to melanin in their cell walls. These fungi, known for their ability to colonise extreme habitats including lichen thalli, are represented by the genus Cladophialophora. In 2023, nine new species of Cladophialophora were described from lichens collected in China, exemplifying the ongoing discovery of novel lichenicolous fungi. These species were isolated from the medullary tissues of various lichen hosts, suggesting potential biotrophic or commensal relationships. Cladophialophora is a lineage of lichenicolous fungi, with many species likely awaiting discovery. The findings add to a growing picture of lichenicolous fungal diversity and illustrate how lichens themselves can serve as refugia for these specialised organisms.
A biological analysis of lichenicolous fungi genera reveals distinct trends. A significant proportion of genera with lichenicolous representatives are exclusively lichenicolous, while others include saprophytic or lichen-forming species as well. For instance, among the lichenicolous Hyphomycetes, 43% of genera are confined to lichens, while for lichenicolous Coelomycetes, this figure rises to 75%.
While the number of known lichenicolous basidiomycete species has increased in recent years, it is believed that many more species remain undiscovered. As of 2022, estimates of global diversity suggest that there are over 1000 species of lichenicolous heterobasidiomycetes, more than 60 species of lichenicolous homobasidiomycetes, and more than 30 species of endolichenic homobasidiomycetes. These estimates are based on analyses of host specificity, current knowledge gaps, and the rate of new species discoveries. The actual number of species may be even higher, especially in under-explored regions and taxonomic groups. Some researchers estimate that the total number of lichenicolous fungal species could potentially reach 3,000.
Taxonomy and nomenclature
The taxonomy and nomenclature of lichenicolous fungi have undergone great changes with the adoption of the "one fungus–one name" principle in the International Code of Nomenclature for algae, fungi, and plants (Melbourne Code). This principle has important implications for classifying and naming lichenicolous fungi. Under the new rules, all legitimate fungal names are treated equally for establishing priority, regardless of the life history stage. This change is significant for lichenicolous fungi, as many species were previously described separately in their sexual (teleomorph) and asexual (anamorph) states.
The implementation of this principle has led to several taxonomic changes. When genetically identical teleomorphs and anamorphs have different names, the older name takes priority, unless the younger name is conserved. For species known only in their anamorphic state, if the teleomorph is discovered, the species is described or combined in the appropriate teleomorph genus, even if teleomorph characters are not mentioned. Anamorphic species recognised as undescribed are now placed in teleomorph genera when their phylogenetic placement is known, rather than in separate anamorphic genera.