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Fantastic Yeasts and Where to Find Them: the Hidden Diversity of Dimorphic Fungal Pathogens

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Fantastic Yeasts and Where to Find Them: the Hidden Diversity of Dimorphic Fungal Pathogens Available online at www.sciencedirect.com ScienceDirect Fantastic yeasts and where to find them: the hidden diversity of dimorphic fungal pathogens 1 1,2 Marley C Caballero Van Dyke , Marcus M Teixeira and 1 Bridget M Barker Dimorphic fungal pathogens are a significant cause of human (see current phylogenetic representation of these species disease worldwide. Notably, the dimorphic fungal pathogens in Figure 1). These fungal organisms are known to be within the order Onygenales are considered primary dimorphic fungal pathogens, which emerged around pathogens, causing disease in healthy hosts. Current changes 150 MYA [1], and are capable of growth in the environment in taxonomy are underway due to advances in molecular on at a wide range of temperatures and in the human host at phylogenetics, population genetics, and new emerging 37 C [2]. Dimorphic fungal pathogens in the order Ony- dimorphic fungal pathogens causing human disease. In this genales are known as primary pulmonary pathogens that review, we highlight evolutionary relationships of dimorphic cause disease in immunocompetent individuals with over fungal pathogens that cause human disease within the order 650 000 new infections occurring each year in the United Onygenales and provide rationale to support increased States [3]. These fungi generally live as saprobes producing investment in studies understanding the evolutionary filamentous mycelium and under certain environmental relationships of these pathogens to improve rapid diagnostics, circumstances produce asexual conidia (e.g. arthroconidia, help identify mechanisms of antifungal resistance, understand blastoconidia, etc.). Upon the inhalation of conidia by a adaptation to human host, and factors associated with susceptible host, these fungi switch into their parasitic form virulence. (e.g. yeasts, spherules, adiaspores, etc.) (Figure 2) and live as endozoans, maintaining an active or inactive stage Addresses within host granulomas. These fungi may return to the 1 Pathogen and Microbiome Institute, Northern Arizona University, environment upon host death transforming into conidia- Flagstaff, AZ, United States 2 producing mycelia [4]. Faculty of Medicine, University of Brası´lia, Brası´lia-DF, Brazil Corresponding author: Barker, Bridget M ([email protected]) Defining pathogenic fungal species based on morpholog- ical characteristics poses many challenges because not all Current Opinion in Microbiology 2019, 52:55–63 fungi are cultivable in media, not all fungal pathogens easily produce sexual fruiting bodies, and some fungi are This review comes from a themed issue on Host–microbe interac- tions: fungi homothallic (self-fertile) and therefore will not exhibit a detectable inheritance pattern. Before the genomic era, Edited by Chad A Rappleye and Duncan Wilson Genealogical Concordance for Phylogenetic Species Rec- For a complete overview see the Issue and the Editorial ognition (GCPSR) was the method of choice for defining Available online 7th June 2019 species boundaries within Onygenales and other fungi https://doi.org/10.1016/j.mib.2019.05.002 [5]. This approach is based on Multi Locus Sequencing 1369-5274/ã 2019 Elsevier Ltd. All rights reserved. Type (MLST) to assess sequence variation of conserved housekeeping genes or other neutral loci. The genetic background of centennial species (i.e. Coccidioides immitis, Paracoccidioides brasiliensis, Histoplasma capsulatum, and Blastomyces dermatitidis) were resolved leading to new phylogenetically isolated species and new dimorphic Introduction fungal pathogens were described (e.g. Emergomyces) [5]. The fungal kingdom contains millions of ubiquitous fungal species, and most pose no or trivial direct threat to human Advances in molecular phylogenetics and population health. However,a handful ofspeciescancausedevastating genetics based on genomic science have significantly disease in both immunocompetent and immunocompro- improved our ability to accurately define fungal species mised individuals. Although plants can also be affected by limits and hybridization events that shaped the Onygen- fungal pathogens, this review highlights a distinct group of alean clade [6]. Sequencing the genomes of Onygenalean dimorphic fungal pathogens that cause disease in humans. fungal pathogens also provides information to better This specificgroupoffungithatcausesystemicinfectionsis understand shared and unique adaptive traits between nested within the order Onygenales (Eurotiomycetes, species complexes, such as metabolism, mating patterns, Ascomycota) which include Coccidioides, Histoplasma, gene gain or loss, and chromosomal variations that may be Blastomyces, Paracoccidioides, Emmonsia, and Emergomyces associated with infection and disease progression [1]. www.sciencedirect.com Current Opinion in Microbiology 2019, 52:55–63 56 Host–microbe interactions: fungi Figure 1 Adiaspore-forming species Ajellomycetaceae Emmonsia crescens Emmonsia sola Blastomyces dermatitidis Blastomyces gilchristii Blastomyces helicus Blastomyces percursus Blastomyces silverae Blastomyces parvus Histoplasma capsulatum (Panama) Histoplasma mississippiense Histoplasma ohiense Yeast-forming 3/13 MYA Histoplasma suramericanum (RJ, LAm A1, LAm A2) species Histoplasma sp. (Eurasia, BAC1, Netherlands, Africa, Australia, LAm B1, LAm B2) Emergomyces africanus Emergomyces canadensis Emergomyces europaeus Emergomyces orientalis Emergomyces pasteurianus Paracoccidioides lutzii Paracoccidioides brasiliensis (S1a, S1b) Paracoccidioides americana 22.5/33 MYA Paracoccidioides restrepiensis Spherule-forming Paracoccidioides venezuelensis species Helicocarpus griseus Polytolypa hystricis Emmonsiellopsis terrestris Emmonsiellopsis coralliformis Arthrodermataceae Coccidioides immitis Coccidioides posadasii 5.1-12.8 MYA Amauroascus mutatus Amauroascus niger Byssoonygena ceratinophila Chrysosporium queenslandicum Ascosphaeraceae Eurotiales Current Opinion in Microbiology Phylogenetic representation of the evolutionary trajectory of the order onygenales. The branch distribution is based on MLST tree (rPB2, TUB2, TEF3, ITS, and LSU), whole genome phylogentic trees, and node calibrations previously published (4200 core genes) [6,61 ,71]. Solid black branches are concordant between both phylogenetic studies and dotted branches are due to uncertainty regarding the true phylogenomic position of Emmonsiellopsis. The solid grey branch represents the outgroup formed by Eurotiales species. The solid red square represents the most common ancestor of Onygenales that emerged around 150 MYA and black ellipsis are nodes distinguishing each lineage. Red nodes represent the age of divergence of each species complex previously analyzed [6,12,37,64]. Blastomyces parvus (*) and Emergomyces pasteurianus (#) were previously known as Emmonsia crescens and E. pasteuriana, respectively. The forms of pathogenic structures among the Onygenales are displayed along the tree. Current Opinion in Microbiology 2019, 52:55–63 www.sciencedirect.com Dimorphic fungi Van Dyke, Teixeira and Barker 57 Figure 2 Environment Host (37°C) Blastomyces Coccidioides Emmonsia Emergomyces Histoplasma Paracoccidioides Current Opinion in Microbiology Morphological shifts of Onygenalean fungi. The simple cartoons for each dimorphic Onygenales are shown. In the environment, each of these species is in its hyphal/mycelial form with oval or circular shapes representing the vegetative conidia. In the case of Blastomyces, Emergomyces, Histoplasma, and Paracoccidioides in the host, these switch to yeast-phase with some characteristic differences. Blastomyces yeast cells display a broad bud neck; Emergomyces have yeast cells with unipolar or bipolar budding at narrow base; Paracoccidioides have yeast that can be multibudded. In the host, Coccidioides switches to endosporulating spherules which then ruptures to release endospores. Emmonsia switches to an adiaspore (non-endosporulating spherule). (Illustration created with BioRender). Additionally, comparative genomic analyses between new estimates suggest 350 000 new infections are occur- pathogenic and non-pathogenic closely related fungal ring each year in the United States [T Chiller, abstract in species provide evidence of recently diverged species Vaccine Strategies for Endemic Fungal Pathogens, and adaptation to mammalian hosts. This review high- NIAID, Rockville, MD, March 2019]. lights studies on the phylogenetics and evolution of dimorphic fungal pathogens, and provides insight into Recently, studies have combined phylogenetic meta- current taxonomy, pathogenicity potential, recombina- analysis and population genetics to identify at least six tion patterns, and gene gain/loss within species distinct populations within the two genetically diverse complexes and across different populations and species. species, C. immitis and C. posadasii [11,12]. C. immitis is restricted to Northwestern Mexico, California, and Coccidioidomycosis Washington. In contrast, C. posadasii is widely distributed Coccidioidomycosis or San Joaquin ‘Valley Fever’ is a in the Americas ranging from the Sonora and Chihuahua fungal infection caused by two Onygenaceae species, deserts (including Arizona, Texas, New Mexico, and C. immitis and Coccidioides posadasii (Figure 1). Coccidioi- Northeast Mexico) to Central and South America. The domycosis occurs most notably in California and Arizona, current understanding of population structure within both which together account for a majority of reported cases in species complexes has been constantly revisited
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