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

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          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.

          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.

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          Most cited references121

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          Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

          Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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            Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

            Some pathogens and pests deliver small RNAs (sRNAs) into host cells to suppress host immunity. Conversely, hosts also transfer sRNAs into pathogens and pests to inhibit their virulence. Although sRNA trafficking has been observed in a wide variety of interactions, how sRNAs are transferred, especially from hosts to pathogens/pests, is still unknown. Here we show that host Arabidopsis cells secrete exosome-like extracellular vesicles to deliver sRNAs into fungal pathogen Botrytis cinerea. These sRNA-containing vesicles accumulate at the infection sites and are taken up by the fungal cells. Transferred host sRNAs induce silencing of fungal genes critical for pathogenicity. Thus, Arabidopsis has adapted exosome-mediated cross-kingdom RNA interference as part of its immune responses during the evolutionary arms race with the pathogen.
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              Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community.

              Pathogens rarely cause extinctions of host species, and there are few examples of a pathogen changing species richness and diversity of an ecological community by causing local extinctions across a wide range of species. We report the link between the rapid appearance of a pathogenic chytrid fungus Batrachochytrium dendrobatidis in an amphibian community at El Copé, Panama, and subsequent mass mortality and loss of amphibian biodiversity across eight families of frogs and salamanders. We describe an outbreak of chytridiomycosis in Panama and argue that this infectious disease has played an important role in amphibian population declines. The high virulence and large number of potential hosts of this emerging infectious disease threaten global amphibian diversity.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mBio
                mBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                5 May 2020
                May-Jun 2020
                : 11
                : 3
                : e00449-20
                Affiliations
                [a ]MRC Centre for Global Infectious Disease Analysis, Imperial College, London, United Kingdom
                [b ]Department of Biosciences, University of Exeter, Exeter, United Kingdom
                [c ]Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA
                [d ]U.S. Geological Survey, National Wildlife Health Center, Madison, Wisconsin, USA
                [e ]Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California—Riverside, Riverside, California, USA
                [f ]Max Planck Fellow Group Environmental Genomics, Max Planck Institute for Evolutionary Biology, Plön, Germany
                [g ]Environmental Genomics, Christian-Albrechts University, Kiel, Germany
                [h ]Max Planck Institute for Terrestrial Microbiology, Department of Organismic Interactions, Marburg, Germany
                [i ]Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada
                [j ]The National Aspergillosis Centre, Wythenshawe Hospital, The University of Manchester, Manchester Academic Health Science Centre, Manchester, United Kingdom
                [k ]Department of Biosciences, University of Exeter, Exeter, United Kingdom
                [l ]Department of Pediatrics, Department of Internal Medicine, and Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin—Madison, Madison, Wisconsin, USA
                [m ]Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, Canada
                [n ]McGill Interdisciplinary Initiative in Infection and Immunology, Departments of Medicine, Microbiology & Immunology, McGill University, Montreal, Canada
                [o ]University of California—Berkeley, Department of Plant and Microbial Biology, Berkeley, California, USA
                [p ]M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, DeGroote School of Medicine, McMaster University, Hamilton, Ontario, Canada
                [q ]Department of Molecular Genetics and Microbiology, Medicine, and Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina, USA
                [r ]Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
                [s ]The Donnelly Centre, University of Toronto, Toronto, Ontario, Canada
                [t ]RIKEN Center for Sustainable Resource Science, Wako, Saitama, Japan
                Vallabhbhai Patel Chest Institute
                Author notes
                Address correspondence to Leah E. Cowen, leah.cowen@ 123456utoronto.ca .
                Author information
                https://orcid.org/0000-0002-1862-6402
                https://orcid.org/0000-0002-5778-960X
                https://orcid.org/0000-0002-7591-0020
                https://orcid.org/0000-0002-2776-5850
                https://orcid.org/0000-0003-4240-6976
                https://orcid.org/0000-0002-9402-9167
                Article
                mBio00449-20
                10.1128/mBio.00449-20
                7403777
                32371596
                aebd0b6c-7890-4984-a3e2-f6e0fbca13f4
                Copyright © 2020 Fisher et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 150, Pages: 17, Words: 13243
                Categories
                Minireview
                Host-Microbe Biology
                Custom metadata
                May/June 2020

                Life sciences
                antifungal resistance,biodiversity,food security,fungal pathogens,global health,medical mycology,plant-pathogenic fungi,wildlife pathogens

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