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Workshop Overview FUNGAL DISEASES: AN EMERGING THREAT TO HUMAN, ANIMAL, AND PLANT HEALTH Will the blight end the chestnut? The farmers rather guess not. It keeps smouldering at the roots And sending up new shoots Till another parasite Shall come and end the blight. —Robert Frost (1936) Fungi are the only group of organisms that have been convincingly shown to cause extinction. —Arturo Casadevall (2010) At the beginning of the 20th century, the American chestnut population counted nearly 4 billion trees. The American chestnut tree, once dominant in the forests of the Eastern United States, was decimated by an accidentally introduced and previously unknown fungal pathogen. Within a span of 40 years, this once abundant, iconic forest tree was all but annihilated by this microscopic fungus. In the middle of the 20th century, an epidemic of Dutch elm disease—a vector-borne fungal disease, also unknown to science at the time—ravaged the elm trees of North America, Europe, and England (Brasier and Buck, 2001). Together, these diseases rapidly and radically transformed the landscape of America’s cities and forests (Money, 2007). 1

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2 FUNGAL DISEASES Fungal diseases of plants, animals, and humans have altered tree population diversity and forest ecosystem dynamics, devastated agricultural crops, triggered global population declines and extinctions in wildlife, and contributed to death and disability in humans. Cryptococcus gattii (C. gattii), a pathogenic fungus that emerged in 1999 on Vancouver Island, British Columbia, Canada, is caus - ing a growing epidemic of human and animal infections and deaths (Galanis and MacDougall, 2010). Since its initial recognition, the pathogen has spread from Vancouver Island to mainland British Columbia and south into the Pacific Northwest of the United States. This fungal pathogen has been associated with 338 confirmed human infections and 40 deaths1 in these regions, which represents the largest documented population of C. gattii infected people in the world (Datta et al., 2009a; Galanis and MacDougall, 2010). Bat white-nose syndrome (WNS) and amphibian chytridiomycosis2 have caused massive population declines and threaten local extinctions of New World bat and amphibian species, respectively (Frick et al., 2010; Skerratt et al., 2007). By 2009, the geographic range of two virulent and highly aggressive strains3 of yellow “stripe” rust—first detected in North America in 2000—expanded to include major wheat-producing areas on five continents, threatening the global wheat supply (Hovmøller et al., 2010). The recent observation that a fungus (Nosema spp.), in combination with a DNA virus, might be associated with “colony collapse” disorder—a disease that has destroyed 20–40 percent of the honeybee colonies in the United States since 2006—underscores the direct and indirect impacts and ecosystem dynamics of fungal diseases in human, plant, and animal communities (Bromenshenk et al., 2010). Fungal organisms interact with humans, animals, and plants in beneficial as well as pathogenic ways. A dozen fungal diseases are considered “life threaten - ing” to humans. At the same time, human health has benefited immensely from fungal-derived antibiotics, such as penicillin (Blackwell et al., 2009; Buckley, 2008; Casadevall, 2007). Indeed, fungi are indispensible to life on this planet through their ability to break down complex organic matter and recycle essential nutrients back into the environment (Wainwright, 1992). The fungal kingdom is among the most diverse kingdoms in the Tree of Life (Blackwell, 2011). Yet, fewer than 10 percent of fungal organisms have been formally described (Hawksworth, 1991, 2001). For the purposes of this chapter, the terms fungi, fungal, and fungus are used inclusively to describe all organisms traditionally studied by mycologists—including species that are now excluded from Kingdom Fungi (e.g., Phytophthora spp. which are members of Oomycota) or whose relationship to the fungal kingdom have yet to be determined (e.g., the 1 As of December 2010. 2 In this chapter, we will refer to this disease as amphibian chytridiomycosis and to the associated pathogen (Batrachochytrium dendrobatidis) as Bd. 3 Puccinia striiformis Westend. f.sp. tritici Eriksson.

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3 WORKSHOP OVERVIEW microsporidia Nosema spp. and the newly discovered cryptomycota) (see Jones et al., 2011; Stajich et al., 2009). Despite the extensive influence of fungi on economic well-being, as well as on human, animal, plant, and ecosystem health, the threats posed by emerging fungal pathogens are often unappreciated and poorly understood. On December 14 and 15, 2010, the Institute of Medicine’s (IOM’s) Forum on Microbial Threats hosted a public workshop on this topic in order to explore the scientific and policy dimensions associated with the causes and consequences of emerging fungal diseases. Through invited presentations and discussions, the workshop explored the environmental, host (plant, animal, and human), and pathogen-related factors influencing the emergence, establishment, and spread of fungal pathogens, as well as the impacts of these diseases on human and animal health, agriculture, and biodiversity. Workshop participants also considered and discussed opportunities to improve surveillance, detection, and response strategies for identifying and mitigating the impacts of these diseases in order to better prepare for future out - breaks. Convened in response to the perceived threat posed by emerging fungal diseases to human, animal, and plant health, this was the first workshop in the Forum’s 15-year history that focused exclusively on fungal pathogens. Organization of the Workshop Summary This workshop summary was prepared by the rapporteurs for the Forum’s members and includes a collection of individually authored papers and commen - tary. Sections of the workshop summary not specifically attributed to an individ- ual reflect the views of the rapporteurs and not those of the Forum on Microbial Threats, its sponsors, or the IOM. The contents of the unattributed sections are based on presentations and discussions at the workshop. The summary is organized into sections as a topic-by-topic description of the presentations and discussions that took place at the workshop. Its purpose is to present lessons from relevant experience, to delineate a range of pivotal is- sues and their respective challenges, and to offer potential responses as discussed and described by the workshop participants. Manuscripts and reprinted articles submitted by some, but not all, of the workshop’s participants may be found, in alphabetical order, in Appendix A. Although this workshop summary provides a description of the individual presentations, it also reflects an important aspect of the Forum’s philosophy. The workshop functions as a dialogue among representatives from different sectors and allows them to present their beliefs about which areas merit further atten - tion. This report only summarizes the statements of workshop participants. This workshop summary report is not intended to be an exhaustive exploration of the subject matter nor does it represent the findings, conclusions, or recommenda - tions of a consensus committee process.

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4 FUNGAL DISEASES THE HIDDEN KINGDOM Fungi are among the most evolutionarily and ecologically diverse organisms on the planet, comprising a kingdom of organisms that provide valuable ecosys - tem services through their decomposition of organic matter, symbiotic associa - tions with numerous plant and animal species, and as food sources (Blackwell, 2011; Taylor et al., 2004). Initially thought by early taxonomists to be members of the plant kingdom, fungi are actually more closely related to animals than plants (Figure WO-1) (McLaughlin et al., 2009). According to keynote speaker Arturo Casadevall, of the Albert Einstein College of Medicine, fungal organisms—in terms of sheer numbers of spe- cies—constitute the most successful kingdom in the tree of life. (Dr. Casadevall’s contribution to the workshop summary report can be found in Appendix A, pages 177–188.) Yet fewer than 10 percent of the estimated 1.5 million species of fungi have been formally identified and described4 (Blackwell, 2011; Hawksworth, 2001). Forum Chair David Relman, of Stanford University, observed that, “We are blind to a lot of their biology and what it is that they spend most of their time doing and why and for whom. I think many in this room would agree that fungi are ignored and underappreciated.” This “blindspot,” he continued, “leaves us with fairly poor situational awareness: a relatively poor understanding of fungal biogeography—meaning their spatial distribution patterns—the factors that de- termine their distribution in space and time, and the factors that underlie their evolution, especially within short time-frames.” Fungal Diversity Existing as single-celled organisms, such as yeasts, or complex communities of filamentous mycelial networks covering hundreds of acres, fungi are ubiqui - tous in nature and display a dazzling array of sizes, shapes, and colors, including many that are bioluminescent (Figure WO-2) (Blackwell, 2011; Desjardin et al., 2010; Lutzoni et al., 2004). The fungal life cycle is equally varied. Fungi can reproduce asexually or sexually through life cycles that range from simple to complex—including “di- morphic” switching between yeast and filamentous forms and the use of multiple host species (Blackwell et al., 2009). Spores5 are produced during the fungal life cycle and may be passively or actively dispersed through a variety of environ- mental media including air, water, wind, animals, and materials (Blackwell et al., 2009). Fungal growth, reproduction, spore production, and dispersal are also ex - quisitely sensitive to environmental conditions including temperature, humidity, 4 This number is considered by many to be an underestimate of the actual number of fungal species; see contributed manuscripts by Blackwell in Appendix A (pages 116–167). 5 Spores are well-protected structures that can survive in adverse environmental conditions, such as freezing or drying (better than mycelia and yeast cells), for months and even years.

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5 WORKSHOP OVERVIEW Animals (outgroup) ? (1 293 642 species) Microsporidia (1300 species) Chytridiomycota (706 species) “ Chytrids” Neocallimastigomycota (20 species) Blastocladiomycota (98 000 species) (179 species) Zygomycota 1 Fungi “ Zygomycetes” ? (327 species) Zygomycota 2 (744 species) Entomophthorales ? (277 species) Glomeromycota (169 species) Ascomycota (64 163 species) Basidiomycota (31 515 species) FIGURE WO-1 The fungal kingdom. The classification of species within kingdom Fungi continues to evolve. The diagram above provides an overview of some of the primary Figure WO-1.eps lineages of fungal organisms and the estimated number of species for each lineage. SOURCE: Blackwell (2010). winds, and water (Bahn et al., 2007; Judelson and Blanco, 2005; Kauserud et al., 2008; Kumamoto, 2008). Fungi are highly adaptable to new environmental niches including what might be considered “extreme” environments (Gostinčar et al., 2010; Le Calvez et al., 2009). Some have suggested the ability of fungi to access multiple strate - gies for reproduction contributes to why fungi are so “adept at adaptation.” Under different environmental conditions, fungal reproduction can maintain character- istics adapted to a particular environmental niche or generate genetically diverse offspring that can quickly respond to changing host or environmental factors (Heitman, 2006). (Dr. Blackwell’s contribution to the workshop summary report can be found in Appendix A, pages 116–167.) Keynote speaker Meredith Black - well, of Louisiana State University, noted that scientists continue to find new species of fungi in a wide range of environments—from tropical and temperate forests to the guts of insects (e.g., Arnold et al., 2003; Gostinčar et al., 2010; Miller et al., 2001; Suh and Blackwell, 2006). These discoveries often reveal the unique capabilities of these microorganisms. As observed by Casadevall, some fungal species can survive and thrive in high radiation and other extreme envi - ronments. Zhdanova et al. (2000) reported extensive fungal growth on the walls

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6 FUNGAL DISEASES A B C D E F G H I . WO-2 new

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7 WORKSHOP OVERVIEW FIGURE WO-2 Diversity of fungal morphology. (A) Two flagellated fungal cells from the recently discovered group of fungi known as cryptomycota. This ancient group of organisms is thought to be distinct from other fungi because of the absence of a cell wall made of chitin; (B) asexual, spore-producing culture of Cryphonectria parasitica (chestnut blight fungus); (C–F) multicellular, spore-producing structures (fruiting bodies) are pro - duced during the sexual phase of the fungal life cycle. Many fruiting bodies are familiar as mushrooms—including species that are consumed by humans as food: (C) Morchella conica (morel) and (D) Crucibulum laeve (bird’s nest fungus). Mushrooms of some species are known to be toxic or poisonous to humans: (E) Amanita muscaria. Fungal fruiting bod- ies can exhibit a wide range of shapes and sizes, including (F) the bioluminescent “shelf” fungus, Panellus stipticus; (G) Micrograph of Phytophthora ramorum chlamydospores; (H) SEM photomicrograph prepared from G. destructans culture isolated from bat tissue samples collected from Williams Hotel Mine; note curved conidia borne in whorls on septate hyphae; bar is 2 µm. All images are pseudo-colored in Adobe Photoshop 9.0; (I) “fairy rings” in which mushrooms sprout along the outer edge of a sprawling, underground mycelial network. These networks (mycelia) have been known to cover several hundred acres. One of largest known mycelia has been estimated to encircle 900 hectares (3.4 square miles). SOURCE: (A) Micrograph kindly provided by Meredith Jones, Exeter University; (B) photo by Kent Loeffler, provided by Alice C.L. Churchill, Cornell University; (C–F) Wi - kimedia Commons; (G) photo provided courtesy of Paul Reeser, Oregon State University; (H) Chaturvedi et al. (2010); (I) Wikimedia Commons. and other areas of the shelter installed around the damaged unit of the Chernobyl nuclear power plant, including 37 species among 19 genera6; fungi are also known to inhabit high-radiation space environments and have even colonized the International Space Station (Dadachova and Casadevall, 2008). The fungal pathogen responsible for sudden oak death and ramorum blight, Phytophthora ramorum, was only identified as a new species in 2000. Since then, according to speaker David Rizzo of the University of California at Davis, researchers have identified an additional 50 Phytophthora7 species. (Dr. Rizzo’s contribution to the workshop summary report can be found in Appendix A, pages 312–324.) As Rizzo observed, these new discoveries do not reflect recent fungal evolution, but are a reflection of the fact that “we just haven’t really been looking 6 Many of the species inhabiting the most heavily contaminated sites of the Chernobyl nuclear power plant were rich in melanin (a high molecular weight pigment). Dadachova et al. (2007) reported that radiation enhances the growth of melanized Wangiella dermatitidis, Cryptococcus neoformans, and Cladosporium sphaerospermum cells. 7 Phytophthora (“plant destroyer”) is a genus of approximately 100 species that includes several notorious plant pathogens, including Phytophthora infestans, which caused the Irish Potato Famine. Phytophthora species are oomycetes, which are fungus-like organisms in the kingdom Stramenopila.

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8 FUNGAL DISEASES for them.” Several other forest fungi that have caused major damage in the past, including the fungi responsible for chestnut blight and Dutch elm disease, were unknown to science until they started causing noticeable damage and die-off of forest and urban trees (Brasier and Webber, 2010). Ecosystem Services8 and Interactions The ability of fungi to process complex organic matter into essential nutrients (e.g., nitrogen, phosphorus) makes them indispensible members of virtually all ecosystems and “invisible” shapers of the world around us (Wainwright, 1992). The vast majority of described fungal species are saprophytic,9 surviving on dead plant matter and animal tissue (Blackwell et al., 2000). Fungi can be “free living”10 or form mutualistic, commensalistic, or parasitic relationships with plants, animals, and microbes—deriving benefits from and contributing to their living hosts (Blackwell et al., 2009). Humans have used fungi as a direct source of food (e.g., truffles, mush - rooms), as a leavening agent for bread, and in the fermentation of various food products, including, but not limited to, beer, wine, and soy products (Buckley, 2008). Some fungi contain psychotropic compounds that may be consumed recreationally or in traditional spiritual ceremonies, and they have been used for millennia for medicinal purposes (Capasso, 1998). The fruiting structures of a few species are highly valued in China for their purported medicinal benefits including as a “libido booster”11 (Roach, 2011). Blackwell stated that since the early 1940s, fungi have been exploited for their life-saving antibiotics. 12 More recently, various enzymes and pigments produced by fungi have been used indus- trially and in the manufacture of a wide variety of products, including furniture, musical instruments, and clothing (Blanchette et al., 1992; Buckley, 2008; Keller et al., 2005). These organisms have been used extensively as biological pesticides to control weeds, plant diseases, and insect pests (Buckley, 2008). Blackwell ob - served that biomedical researchers have used certain species of fungi extensively as model organisms for genetic and other scientific research for decades. Many fungi maintain close associations with their insect hosts. Blackwell discussed the symbiotic fungi that inhabit insect guts and are essential to the 8 Services provided by ecosystems that benefit humans and are necessary for a healthy planet like oxygen production, water purification, pollination, soil formation, and nutrient recycling. See www. conservation.org/resources/glossary/Pages/e.aspx (accessed on June 13, 2011). 9 Deriving nutrients from dead organic matter. 10 Not dependent on a host for survival. 11 For example: A parasitic fungus, Ophiocordyceps sinensis, grows in the Tibetan Plateau in China and is highly valued for its “purported medicinal benefits,” including uses as “a treatment for cancer and aging and as a libido booster.” The nutty-tasting fungus is considered “fungal gold” because it can be sold for high prices in Chinese markets (see Roach, 2011). 12 Other medicines such as the immunosuppressant cyclosporine A and statin drugs also are derived from fungi.

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9 WORKSHOP OVERVIEW nutrition of many insects (e.g., Nardi et al., 2006; Suh et al., 2003, 2005). Fungi also are cultivated by fungus-farming termites and ants (Aanen et al., 2002; Currie et al., 2003; Dentinger et al., 2009; Munkacsi et al., 2004) (Box WO-1). Not all fungal–insect associations are mutualistic. Blackwell described the parasitic but not usually pathogenic fungi in the order Laboulbeniales. She noted the reports of extreme host specificity exhibited by different species in this order—sometimes inhabiting only certain parts of the host insect (Weir and Beakes, 1995). Most laboulbenialean species are associated with beetles (Cole - optera), and flies (Diptera), but they are also associated with a diverse array of host species in other insect orders, mites and millipedes (Weir and Beakes, 1995). Blackwell discussed a number of fungal–plant symbioses. She estimated that: • Half of all ascomycetes (Phylum Ascomycota) are lichens [symbiotic associations between fungi and photosynthetic partners (algae)] (Lutzoni et al., 2001; Schoch et al., 2009); • 90 percent of all photosynthetic plants have mycorrhizal associates (Ruehle and Marx, 1979); and • 95 percent of all plants have fungal endophytes (Arnold, 2007; Rodriguez et al., 2009). Endophytes—fungi that live inside the plant tissue but without causing any obvious negative effects—are less well known than other plant–fungal as - sociations, but mycologists find them wherever they look (Arnold et al., 2003; Rodriguez et al., 2009). Numerous endophytic fungal infections have been ob - served in cocoa trees (Theobroma cacao) and they may play an important role in host defense by decreasing the damage associated with Phytophthora spp. infections (Arnold et al., 2003). To illustrate the complexity of these relationships, Blackwell noted interactions among the fungus Curvularia protuberata, the grass Dichanthelium lanuginosum,13 and a fungal virus. The grass infected with the fungus infected with “Curvularia thermal tolerance virus” provides thermal re- sistance benefits for the host plant. This tripartite relationship allows the grass to grow in the high-temperature soils of Yellowstone National Park (Márquez et al., 2007). Blackwell pointed to the red-cockaded woodpecker (Picoides borealis) as just one example of the many ways that fungi confer benefits to the health of ecosystems. These woodpeckers usually nest in trees infected with red heart rot (Phellinus pini) (Hooper et al., 1991). 13 Commonly referred to as Panic Grass.

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10 FUNGAL DISEASES BOX WO-1 The Fungal Gardens of Leafcutter Ants Over the past 50 million years, a unique symbiosis has developed between attine (fungal growing) “leafcutter” ants and fungi in the Lepiotacea family. In what biologists consider the earliest form of agriculture, leafcutter ant colonies grow and meticulously maintain a specific fungal cultivar for food (Schultz and Brady, 2008; Wade, 1999). Inhabiting forest ecosystems throughout Mexico and Central and South Amer- ica, these ant colonies can number more than 8 million individuals. Foraging ants bring cut pieces of leaves back to the colony where they are broken down and fed to the fungus by worker ants (see Figure WO-1-1). A second symbiotic relationship protects these fungal gardens. Pseudono- cardia bacteria, which grow on the bodies of the worker ants, produce antibiotic compounds that prevent the growth of parasitic molds (Currie et al., 1999). FIGURE WO-1-1 Leafcutter ants tending their fungal garden. Figure WO- figure for Box WO-1.eps SOURCE: © Alex Wild. For more information on leafcutterbitmap the PBS video ants, visit segment: “Ancient Farmers of the Amazon,” © WGBH Educa- tional Foundation and Clear Blue Sky Productions, Inc., 2001, available at: http://www.youtube.com/watch_popup?v=RH3KY BMpxOU&vq=medium#t=11. Or, use your smart phone to link directly to the video using the QR code at right: Figure WO-QRtode.eps bitmap

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11 WORKSHOP OVERVIEW Fungi as Pathogens The longstanding utility of fungi to all life on earth has often been matched by their ability to directly or indirectly cause devastating disease in human, animal, and plant hosts. Fungi are the predominant pathogen species in plants, remarked Casadevall, and fungi can also cause disease in healthy humans and animals. Described by several workshop participants as “formidable pathogens,” many fungi can also endure adverse environmental conditions and thrive outside of their host (Casadevall, 2007). Fungal pathogens in general execute a series of sequential steps in order to cause disease, remarked speaker Barbara Howlett of the University of Melbourne. (Dr. Howlett’s contribution to the workshop summary report can be found in Ap - pendix A, pages 264–273.) These pathogens must: • Recognize and attach to the host; • Germinate, colonize, and derive nutrition from the host; • Subvert host defense responses; • Reproduce, exit, and disperse; and Find another host14 (Sexton and Howlett, 2006). • Very few fungal pathogens are able to cause disease in hosts from the plant and animal kingdoms; those that do are referred to as trans-kingdom pathogens (De Lucca, 2007).15 Fungi can also form different associations with different host types. For example, the fungus Cryptococcus gattii is pathogenic in animals in- cluding humans, but forms non-pathogenic associations with plants –which play an essential role in the maintenance of C. gattii spores in certain environmental niches (Bartlett et al., 2007; Xue et al., 2007).Once outside of a host, fungal pathogens of animals and plants often have different requirements for survival. Animal pathogens, noted Howlett, are often soil saprophytes that are free-living rather than obligate.16 In contrast, some plant pathogens can only survive on the tissue of a specific plant host(s). 14 For more information, see contributed manuscript by Barbara Howlett in Appendix A (pages 264–273). 15 Howlett noted two trans-kingdom pathogens during her remarks: Fusarium oxysporum f. sp. lycopersici, which causes vascular wilt in plants and is an emerging human pathogen (Ortoneda et al., 2004); and Aspergillus flavus, which infects corn and is an emerging pathogen in immunocompro- mised humans (Krishnan et al., 2009). 16 Capable of existing only in a particular environment; an obligate parasite cannot survive inde - pendently of its host (Science dictionary).

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