Speleomycology – fungi in underground ecosystems
Rafał Ogórek, Justyna Borzęcka, Agata Piecuch, Mateusz Speruda, Department of Mycology and Genetics, Institute of Genetics and Microbiology, University of Wroclaw, Przybyszewskiego Street 63/77, 51-148 Wrocław, Poland
Caves, mines, and other underground objects are usually associated with mining industry or as hideaways both for animals and for humans in the old days. Currently, they became a great tourist attraction for visual (e.g., speleothems) and cultural reasons. We often forget that microorganisms can also be present in this type of places, among which microscopic fungi are one of the most important.
The studies of microscopic fungi and mushrooms in underground ecosystems are conducted by speleomycological methods. The scope of this research includes the determination of the number of spores and other organs forming fungal colonies (among others, those inhabiting rocks, water, air, organic matter, and animals living in underground ecosystems), as well as the control of factors affecting the occurrence of fungi in these objects. An important issue is also the monitoring of fungal spores suspended in the air in order to determine the biological safety of a given object. In underground ecosystems, it is common to find microscopic fungi, while fruiting bodies and spores of macroscopic fungi are very rarely discovered there. It should be noted that mycological studies of underground objects have been performed since the 1960s, but the term “speleomycology” was first used in world literature in 2014 in the work entitled Speleomycological research in underground Osówka complex in Sowie Mountains (Lower Silesia, Poland). This concept was introduced by Polish researchers: Wojciech Pusz and Rafał Ogórek.
Underground ecosystems are very unique places due to their specific microclimate, including high air humidity, often reaching 100%, persistently low temperature, lack of light, and low abundance of organic matter. These conditions are unfavorable for the occurrence and development of most organisms. Therefore, the majority of underground objects are described as heterotrophic ecosystems, meaning incomplete ecosystems devoid of producers; which lack self-sufficiency. All matter occurring in these ecosystems is carried from the outside and comes from the excrement and remains of animals present there, such as bats. Obviously, there are exceptions to this rule. One of them is the Movile Cave (Romanian: Peştera Movile) in Romania, with chemolithoautotrophic ecosystem. This cave has a unique underwater ecosystem, rich in hydrogen sulfide and carbon dioxide with a very low oxygen content. It is estimated that life in this facility has been isolated from the outside world for the last 5.5 million years.
The specific microclimate of underground objects also influences the form of occurring microorganisms, especially microscopic fungi. Most microorganisms do not actively grow in this type of ecosystem, but they, as well as the compounds they secrete, may be present in bioaerosols, i.e. the biological fraction of air. Airborne fungi may have a negative impact on human and animal health, both in terms of exceeding general quantitative standards (the number of spores in 1 m3 of air) and the presence of specific taxa. A good example is the genus Cladosporium or Alternaria, commonly found in the atmospheric air (as well as underground), which can cause allergies in sensitive individuals. That is why the aforementioned aeromycological monitoring of underground facilities is so important. In turn, Pseudogymnoascus destructans (formerly known as Geomyces destructans) is responsible for causing white-nose syndrome in bats (WNS). This fungus attacks bats hibernating in the underground sites by growing on their wing membranes and mouth. As a consequence, this leads to a loss of body fat and weight, dehydration, electrolyte imbalance, hyperactivity during the winter, and ultimately death. Particularly in the USA and Canada, a mass plague of these small mammals due to infection by P. destructans has been reported. It should be noted, however, that fungi also have a beneficial effect on underground ecosystems, and it is difficult to imagine life without their presence in such facilities.
When speaking about the presence of fungi in underground ecosystems, one should mention geomycology. The concept itself was introduced into the literature in order to distinguish between the geological processes taking place with the participation of fungi and those involving mainly bacteria (geomicrobiology). Thus, geomycology mainly deals with the effects of fungi on geological processes, including weathering of rocks and minerals, metal accumulation, and the fungal contribution to the circulation of elements and nutrients. Fungi can affect rocks and other mineral substrates in a biochemical and/or biomechanical way. The first of these activities consists in the release of various compounds into the environment by fungi, e.g., acids, dyes, and metal chelating compounds. On the other hand, biomechanical activity is of little importance and concerns mainly limestone rocks. It involves the mechanical penetration of mineral substrates by fungi through the production of hyphae.
From the underground objects, fungi belonging to the Ascomycota group (sac fungi) are isolated most frequently, which account for 69.1% of all fungi obtained. Fungi belonging to this group are common in the environment. The following clusters are 20.0% Basidiomycota (basidiomycetes), 6.6% Zygomycota (zygomycetes), 2.6% Mycetozoa (slime molds), 1.0% Oomycota (oomycetes), and 0.8% others. In turn, the most common types of fungi in the underground environment are Aspergillus, Penicillium, Mucor, Fusarium, Trichoderma, Cladosporium, Alternaria, Paecilomyces, Acremonium, Chrysosporium, Laboulbenia, Rhizopus, Mortierella, and Chaetomium. Additionally, in the presence of bats and their excrements in the underground, species classified as Pseudogymnoascus, Histoplasma, and Geomyces may appear. Although speleomycological research has been conducted for several decades, many groups of fungi are still not well known. Examples include dermatophytes, species that cause mycoses of the skin and its appendages (hair and nails). So far, it has been found that dermatophytes such as Artroderma curreyi, Artroderma quadrifidum, Microsporum gypseum, Trichophyton mentagrophytes, Trichophyton rubrum, and Trichophyton terrestre may occur in underground objects
Underground ecosystems are wonderful places in terms of visual, cultural, and biological value. Animals and their microorganisms are unique and very often produce specific mechanisms that allow them to survive or live in such extreme conditions. The issues related to speleomycology, i.e. fungi in underground ecosystems, seem to be particularly interesting and still little known. On the one hand, these organisms exert an invaluable influence on life in underground facilities, but on the other hand, they can pose a biological threat to other living organisms.