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Crossover Fungal Pathogens: the Biology and Pathogenesis of Fungi

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Crossover Fungal Pathogens: the Biology and Pathogenesis of Fungi YFGBI 2598 No. of Pages 12, Model 5G 12 September 2013 Fungal Genetics and Biology xxx (2013) xxx–xxx 1 Contents lists available at ScienceDirect Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi 5 6 3 Crossover fungal pathogens: The biology and pathogenesis of fungi 4 capable of crossing kingdoms to infect plants and humans ⇑ 1 7 Q1 Gregory M. Gauthier , Nancy P. Keller 8 University of Wisconsin – Madison, Madison, WI, USA 9 10 article info abstract 2412 13 Article history: The outbreak of fungal meningitis associated with contaminated methylprednisolone acetate has thrust 25 14 Available online xxxx the importance of fungal infections into the public consciousness. The predominant pathogen isolated 26 from clinical specimens, Exserohilum rostratum (teleomorph: Setosphaeria rostrata), is a dematiaceous 27 15 Keywords: fungus that infects grasses and rarely humans. This outbreak highlights the potential for fungal patho- 28 16 Crossover fungi gens to infect both plants and humans. Most crossover or trans-kingdom pathogens are soil saprophytes 29 17 Q3 Trans-kingdom fungi and include fungi in Ascomycota and Mucormycotina phyla. To establish infection, crossover fungi must 30 18 Plant pathogenic fungi overcome disparate, host-specific barriers, including protective surfaces (e.g. cuticle, skin), elevated tem- 31 19 Human pathogenic fungi perature, and immune defenses. This review illuminates the underlying mechanisms used by crossover 32 20 Pathogenesis 21 Iron fungi to cause infection in plants and mammals, and highlights critical events that lead to human infec- 33 22 Velvet protein complex tion by these pathogens. Several genes including veA, laeA, and hapX are important in regulating biolog- 34 23 ical processes in fungi important for both invasive plant and animal infections. 35 Ó 2013 Published by Elsevier Inc. 36 37 38 39 1. Introduction highlights the ability for a subset of fungal pathogens to cause 56 infection in members of plant and animal kingdoms. 57 40 The outbreak of meningitis associated with contaminated Human fungal infections range from superficial nail and skin 58 41 methylprednisolone acetate from the New England Compounding infections (1.7 billion infections/year worldwide) to mucocutane- 59 42 Center has thrust the importance of invasive fungal infections into ous candidiasis (>85 million infections/year worldwide) to invasive 60 43 the public consciousness (reader is referred to companion piece by fungal infections (>2 million infections/year worldwide) (Brown 61 44 Andes and Casadevall, also Kainer et al., 2012; Smith et al., 2012). et al., 2012). Invasive fungal infections (IFI) in humans typically af- 62 45 Exserohilum rostratum (teleomorph: Setosphaeria rostrata), which fect persons with impaired immunity such as those undergoing so- 63 46 belongs to a group of dematiaceous (highly melanized) fungi that lid organ or hematopoietic stem cell transplantation. In this 64 47 cause necrosis of grasses (leaf spot, crown and root rot; reader is population, the incidence of IFIs is increasing (Pappas et al., 65 48 referred to companion piece by Turgeon), is the predominant 2010; Kontoyiannis et al., 2010; Bitar et al., 2009). The establish- 66 49 organism isolated from patient samples (Smith et al., 2012; Pratt, ment of the transplant-associated infection surveillance network 67 50 2005, 2003). Moreover, other potential phytopathogens (e.g., Clad- (TRANSNET), which tracks IFIs in the United States, has enabled a 68 51 osporium cladosporioides, Rhizopus stolonifer) have been identified deeper understanding of the epidemiology of fungal pathogens. 69 52 in contaminated methylprednisolone lots (Smith et al., 2012; In solid organ transplant recipients (SOT), Candida spp. (53%) and 70 53 Holmes, 2002; CDC). Before this outbreak, human E. rostratum Aspergillus fumigatus (19%) are the most common agents of IFI; 71 54 infections were rarely reported in the medical literature and lim- whereas dematiaceous fungi, Fusarium spp., mucormycetes, and 72 55 ited to persons with impaired immunity. Moreover, this outbreak other molds collectively represent 10% of IFIs (Pappas et al., 73 2010). In hematopoietic stem cell transplant (HSCT) recipients 74 Aspergillus fumigatus (44%) and invasive Candida spp. (28%) are 75 the most common pathogens (Kontoyiannis et al., 2010). IFI from 76 ⇑ Corresponding author. Address: Department of Medicine, Section of Infectious mucormycetes (8%), dematiaceous fungi (7%), Fusarium spp. (3%), 77 Q2 Diseases, School of Medicine and Public Health, University of Wisconsin – Madison, 78 1550 Linden Drive, Microbial Sciences Building, Room 3472, Madison, WI 53706, and unspecified molds (6%) occur at a higher frequency in HSCT USA. Fax: +1 (608) 263 4464. recipients than SOT recipients. Although non-Candida, non-Asper- 79 E-mail addresses: [email protected] (G.M. Gauthier), [email protected] gillus fungi represent a small proportion of IFIs, mortality associ- 80 (N.P. Keller). ated with these pathogens is substantial—39% mortality for SOT 81 1 Current address: Department of Medicine and Public Health, Department of recipients and 72–95.7% mortality for HSCT recipients (Pappas 82 Medical Microbiology, University of Wisconsin – Madison, 1550 Linden Drive, 83 Microbial Sciences Building, Room 3476, Madison, WI 53706, USA. et al., 2010; Kontoyiannis et al., 2010). 1087-1845/$ - see front matter Ó 2013 Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fgb.2013.08.016 Please cite this article in press as: Gauthier, G.M., Keller, N.P. Crossover fungal pathogens: The biology and pathogenesis of fungi capable of crossing king- doms to infect plants and humans. Fungal Genet. Biol. (2013), http://dx.doi.org/10.1016/j.fgb.2013.08.016 YFGBI 2598 No. of Pages 12, Model 5G 12 September 2013 2 G.M. Gauthier, N.P. Keller / Fungal Genetics and Biology xxx (2013) xxx–xxx 84 Epidemiologic data for agriculture fungal pathogens on a na- Ungerminated conidia of plant pathogenic fungi attach to the 146 85 tional scale is hindered by the complexity of monitoring diverse cuticle, which forms a hydrophobic surface composed of hydroxyl 147 86 types of food crops and limited resources for diagnostic testing. and epoxy fatty acids (C16,C18), waxes (epicuticular, intracuticu- 148 87 Thus, knowledge is primarily limited to large outbreaks of disease lar), phenolic compounds (e.g., cinnamic acids, flavonoids, lignins), 149 88 and global monitoring of wheat rust pathogens. Outbreaks of agri- and polysaccharides (Dominguez et al., 2011). The cuticle covers 150 89 cultural fungal pathogens are multifactorial in etiology and can in- stems, leaves, fruits, flowers, and seeds to protect the plant against 151 90 volve introduction of a novel pathogen, increased host susceptibility biotic and abiotic stresses (Dominguez et al., 2011). Conidial adhe- Q4 152 91 from reduced genetic diversity, and changes in climate (Vurro et al., sion prevents displacement by water or wind currents, and is asso- 153 92 2010). Cochliobolus species have been responsible for widespread ciated with germination and invasion (Mercure et al., 1994a,b). 154 93 destruction of important agriculture crops such as corn, which has Colletotrichum graminicola conidia adhere to plant tissues using a 155 94 resulted in famine and economic instability (Rossman, 2009). Global multi-stage process that involves (i) attachment of ungerminated 156 95 monitoring of the pathogens responsible for stem (Puccinia gramin- conidia to hydrophobic surfaces within 30 min of contact; (ii) re- 157 96 is), leaf (Puccinia triticina, Puccinia tritici-duri), and yellow (Puccinia lease of a glycoprotein containing matrix at the site of conidial 158 97 striiformis) rust diseases of cereal crops using field surveys has facil- attachment; and (iii) strengthening of the initial attachment by re- 159 98 itated interventions to minimize economic losses, which can be lease of glycoproteins from the appressorium (Mercure et al., 160 99 substantial—U.S. $1.12 billion/year (Pardey et al., 2013; Park et al., 1994a,b; Mercure et al., 1995; Sugui et al., 1998). Mucilage associ- 161 100 2011). In the United States, the establishment of the National Plant ated with conidial production provides protection from dessication 162 101 Diagnostic Network by the Agricultural Bioterrorism Act of 2002 (in but does not promote attachment to plant surfaces (Mercure et al., 163 102 response to the 9/11 terrorist attacks), has facilitated identification 1994a,b). Similarly, Fusarium solani conidia release an extracellular 164 103 and tracking of emerging plant pathogens including Phakopsora matrix upon contact with plant surfaces (Kwon and Epstein, 1997). 165 104 pachyrhizi, the etiologic agent of soybean rust. Within this matrix is a 90 kDa glycoprotein (mannoprotein) that is 166 105 Of the 1.5–5.1 million fungal species, an estimated 270,000 spe- postulated to function as an adhesin (Kwon and Epstein, 1997). 167 106 cies are associated with plants and 325 are known to infect hu- Attachment by this glue-like mechanism is shared by other patho- 168 107 mans (Blackwell, 2011; Hawksworth and Rossman, 1997; Robert genic ascomycetes including Magnaporthe oryzae (etiologic agent 169 108 and Casadevall, 2009; Woolhouse and Gaunt, 2007). A small subset of rice blast disease) and Blumeria graminis (powdery mildew of 170 109 of plant pathogens such as E. rostratum can cross kingdoms and in- cereals and grasses), and aquatic saphrophytes such as Lemonniera 171 110 fect humans. These crossover pathogens
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