Threats Posed by the Fungal Kingdom to Humans, Wildlife, and Agriculture

Abstract

The fungal kingdom includes at least 6 million eukaryotic species and is remarkable with respect to its profound impact on global health, biodiversity, ecology, agriculture, manufacturing, and biomedical research. Approximately 625 fungal species have been reported to infect vertebrates, 200 of which can be human associated, either as commensals and members of our microbiome or as pathogens that cause infectious diseases. These organisms pose a growing threat to human health with the global increase in the incidence of invasive fungal infections, prevalence of fungal allergy, and the evolution of fungal pathogens resistant to some or all current classes of antifungals. More broadly, there has been an unprecedented and worldwide emergence of fungal pathogens affecting animal and plant biodiversity. Approximately 8,000 species of fungi and Oomycetes are associated with plant disease. Indeed, across agriculture, such fungal diseases of plants include new devastating epidemics of trees and jeopardize food security worldwide by causing epidemics in staple and commodity crops that feed billions. Further, ingestion of mycotoxins contributes to ill health and causes cancer. Coordinated international research efforts, enhanced technology translation, and greater policy outreach by scientists are needed to more fully understand the biology and drivers that underlie the emergence of fungal diseases and to mitigate against their impacts. Here, we focus on poignant examples of emerging fungal threats in each of three areas: human health, wildlife biodiversity, and food security.

Keywords: antifungal resistance; biodiversity; food security; fungal pathogens; global health; medical mycology; plant-pathogenic fungi; wildlife pathogens.

FIG 1

The drivers of emerging fungal threats to plants and animals. Four key factors favor the emergence of fungi that infect plants and animals. (i) Evolutionary potential (blue boxes). High pathogen abundance and virulence enhance evolutionary potential. A rapid and repeating life-cycle generates a large pathogen population density. High genetic strain diversity hastens emergence of novel fungal genotypes and lineages, with diversity generated by enhanced reproductive capacity (sexual, parasexual, or clonal), whole-genome or hyphal fusions (144), or genome plasticity endowed by aneuploidy/copy number variation (145), horizontal gene transfer (146), or two-speed genomes (147). (ii) Artificial selection and host susceptibility (gray boxes). A homogeneous host, such as a large population of animals or a crop monoculture, fuels pathogen variant emergence. Fungicide-resistant genotypes emerge due to protracted and repeated treatments/sprays and via the dual use of antifungals on crops and in the clinic (18). (iii) Dispersal/epidemiology (red boxes). Pathogens and infected hosts are disseminated globally via movement of infected biota (85), contamination of traded goods, or long-distance spore dispersal by, for example, airplanes or vectoring by hurricane winds (119, 148). Fungi can persist long-term as resting spores or via saprophytic growth. They can hop hosts or persist as generalist pathogens by causing infections on multiple hosts (18). Transmission can be enhanced by extended phenotypes (149), while coinfections, polyparasitism, and transkingdom interactions can mitigate or fuel the emergence of novel strains) (85). (iv) Environmental permissiveness (green boxes). Anthropogenic and meteorological amplifiers of fungal pathogen emergence include population growth, changing population demography fueled by urbanization or conflict, aging, immunosuppression, and nosocomial hospital-acquired infections. A warming world, with increased incidences of dramatic/extreme weather events and a change in the amounts of, for example, CO₂ and N₂O (150), has the potential to further fuel the emergence of fungal pathogens.