The future is now: How to conserve fungi

Fungi, a group of eukaryotic kingdom, are one of the most speciose and widely distributed life forms on the earth. It is estimated that 2–3 million fungal species are distributed all over the world but with more than 90% of this number awaiting to be described.1 Fungi exist in all natural environments, from humid tropical rainforests to arid deserts and even in the extreme cold earth's poles, and also can form symbiotic and pathogenic networks with other life forms. Fungi are closely related to human beings, and thus can be treated as a kind of strategic biological resources.2 For example, yeasts are crucial for fermenting various foods and drinks, and medicinal macrofungi, like Ganoderma lingzhi, have been utilized for thousands of years in traditional medicines and folk culture as a symbol of good fortune all over the world. On the other hand, human activity to some extent has shaped fungal diversity and distribution. In the Anthropocene, the man-made material plastic provides a unique niche for the directional selection of fungi, and the global warming resulting from the greenhouse effect releases fungi from the cryosphere into human habitats. Moreover, the artificial destruction of natural environments may have caused the extinction of many fungal species before their description. Therefore, for future utilization, it is now urgent to recognize and conserve fungi. Compared with animals and plants, fungi receive less attention partially due to the fact that macrofungi have a stage during their whole life history as an invisible mycelial form and microfungi are generally invisible throughout their life history to the naked eye. Besides the low proportion of described species to estimated species, fungal distribution, trait evolution and spatiotemporal patterns are also much less known than animals and plants. This knowledge gap restricts formulating effective policy for fungal conservation, and thus needs to be filled (Figure 1). The knowledge gap needs to be filled for fungal conservation. To conserve fungi, the highest priority is to recognize fungi. At least three dimensions are worthy of attention at the species level. Following the International Code of Nomenclature for algae, fungi, and plants (ICNafp), real materials are required for formally naming fungal species. Under ICNafp, about 2–3 thousand fungal species were newly described per year in last dozens of years. At this rate of description, it will take 1000 years to name all of the estimated species. Even though the DNA sequence data can be accepted as a category of nomenclatural type in the near future,3 the traditional voucher-based method may still be used for visible and culturable fungi. In addition, the method using DNA sequence data as the type itself is also time-consuming. Therefore, it is impossible to name all species following a standard taxonomic practice in a reasonable time. Then, the fungi in special niches, like cryosphere and plastisphere, and unique evolutionary position, like chytrids in the basal lineages, should be primarily focused on. These fungal species will help us understand the impact of human activities on fungi, and the reason why fungi are so speciose. Besides describing new species, it is also important to repeatedly record as many known fungal species as possible. The related records at least include the occurrences, geographic distribution, phenotypic variants, and genetic differences among various individuals of a single species. This basic data will facilitate comprehensive recognition of fungal species. Unfortunately, most fungal taxonomists normally neglect known species on field trips and in laboratory experiments. Instead, they are keen to describe new species and then leave them behind to describe other new species again and again. Among others, one typical indication of this phenomenon is the rare records of fungi in the Global Biodiversity Information Facility. The application potential of fungi is as important as their natural attribute with regard to recognizing fungi. Indeed, it is the potential itself that motivates us to explore the diverse fungal world. For now, only a handful of known fungal species are subjected to realistic utilization. Nevertheless, this small amount of fungi has extremely benefited to human beings in various ways.4 To further utilize fungal resources, more and more fungi, both known species and newly described species, should be involved in experiments to determine whether they have potentials in synthesizing medicines, degrading wastes, enhancing agricultural productivity, improving food quality and so on. The taxonomic position and multiomics information of fungal species may provide clues for their application potential, but more data still need to be accumulated for precise prediction. Based on the above-mentioned fundamental data of fungi, appropriate analyses will provide crucial directions for fungal conservation at different dimensions. At the species level, the International Union for Conservation of Nature provides a global red list of fungi, and approximately 58 countries have their own official or unofficial national red lists. However, the number of species recorded in these lists is extremely low: only 0.4% of known species. This phenomenon is mainly due to that the available information on most known fungi is not sufficient to be evaluated. In addition, the red lists are evaluated mainly on the basis of fungal occurrences and geographic distribution. In our opinion, more related data, including but not limited to phylogenetic diversity and application potentials, should also be considered. Then, a checklist of strategic fungal resources with weighted scores for each species will be generated, which will provide prior species for conservation. One thing to be clarified is that the pathogens, if preserved appropriately, may be important biological resources for scientific research, but they are not in the scope of the current fungal conservation in the wild. Enlarging to the group level, viz. a group of fungi with the most recent common ancestor, it is rare to explore how the speciose fungi diversify and what biological traits facilitate the diversification. The current knowledge indicates that the diversification of mushroom-forming fungi in the class Agaricomycetes is associated with the adaptive radiation of morphological and trophic traits to niches at different time range.5 This is a significant contribution to fungal evolution, but the studies focusing on such a large taxonomic scale cannot comprehensively sample taxa for evolutionary analyses. Moreover, at finer evolutionary scales, the driving force of adaptive evolution to fungal diversification is less concerned. Therefore, much more evolutionary works on various fungal groups need to perform with comprehensive sampling. Then, the understanding of evolutionary history will reveal certain fungal groups with a higher rate of diversification. This high evolutionary and diverse potential deserves prior conservation. To conserve biodiversity, the most important thing is to conserve the habitats. Some countries have established national parks and nature reserves. These efforts definitely promote the conservation of biodiversity. However, these parks and reserves are rarely specific for fungal conservation. Therefore, it is critical to select prior regions special for fungal conservation. Firstly, a preliminary but systematic investigation on fungal diversity is necessary. Then, according to the data of species richness, occurrences and geographic distribution, community phylogenetics and spatiotemporal patterns with an emphasis of prior fungal groups can be analyzed. The generated regions with higher species and phylogenetic diversity and more rapid recent speciation deserve priority in terms of fungal conservation. Besides, the regions conceiving abundant prior fungal species and groups should also have a higher priority. Eventually, the prior regions for fungal conservation can be selected, where some permanent sample plots should be set up for the long-term monitoring of fungi. The accumulated information year by year will provide robust background data for proposing theories of fungal conservation biology. With the guidance of the theories, the prior species can be preferentially preserved in fungaria and culture collection centers, and the preserved fungal strains may be released back into the wild. In summary, to save the future of fungi and also human beings, we need to act now. With the advanced technology of molecular sequencing and remote sensing, the comprehensive fungal information needs to be recorded, and the application potentials of recorded fungi are better to be determined. From the fundamental data, the prior species, groups and regions for fungal conservation can be selected via appropriate analyses. Hopefully, a long-term monitoring in permanent sample plots will be launched soon by policy makers, which may help to propose theories of fungal conservation biology. Shi-Liang Liu: Visualization; writing - original draft; conceptualization. Dong-Mei Liu: Conceptualization. Li-Wei Zhou: Conceptualization; supervision; writing - review & editing; writing - original draft; funding acquisition. The research was financed by the National Key Research and Development Program of China (No. 2022YFC2601200).