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The Global Epidemiology of Emerging Histoplasma Species in Recent Years

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The Global Epidemiology of Emerging Histoplasma Species in Recent Years available online at www.studiesinmycology.org STUDIES IN MYCOLOGY xxx: xxx (xxxx). The global epidemiology of emerging Histoplasma species in recent years Anderson Messias Rodrigues1*, Mathew A. Beale2, Ferry Hagen3,4,5, Matthew C. Fisher6, Paula Portella Della Terra1, Sybren de Hoog3, Raimunda S^amia Nogueira Brilhante7, Rossana de Aguiar Cordeiro7, Debora de Souza Collares Maia Castelo-Branco7, Marcos Fabio Gadelha Rocha8, Jose Júlio Costa Sidrim7, and Zoilo Pires de Camargo1* 1Laboratory of Emerging Fungal Pathogens, Department of Microbiology, Immunology and Parasitology, Federal University of S~ao Paulo, S~ao Paulo, 04023-062, Brazil; 2Parasites and Microbes Programme, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, CB10 1SA, UK; 3Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands; 4Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, The Netherlands; 5Laboratory of Medical Mycology, Jining No. 1 People's Hospital, Jining, Shandong, People's Republic of China; 6MRC Centre for Global Infectious Disease Analysis, School of Public Health, Imperial College London, London, UK; 7Specialized Medical Mycology Center, Postgraduate Program in Medical Microbiology, Federal University of Ceara, Fortaleza, Ceara, Brazil; 8Postgraduate Program in Veterinary Science, State University of Ceara, Fortaleza, Ceara, Brazil *Correspondence: Anderson Messias Rodrigues, [email protected]; Zoilo Pires de Camargo, [email protected] Abstract: Histoplasmosis is a serious infectious disease in humans caused by Histoplasma spp. (Onygenales), whose natural reservoirs are thought to be soil enriched with bird and bat guano. The true global burden of histoplasmosis is underestimated and frequently the pulmonary manifestations are misdiagnosed as tuberculosis. Molecular data on epidemiology of Histoplasma are still scarce, even though there is increasing recognition of histoplasmosis in recent years in areas distant from the traditional endemic regions in the Americas. We used multi-locus sequence data from protein coding loci (ADP-ribosylation factor, H antigen precursor, and delta-9 fatty acid desaturase), DNA barcoding (ITS1/2+5.8s), AFLP markers and mating type analysis to determine the genetic diversity, population structure and recognise the existence of different phylogenetic species among 436 isolates of Histoplasma obtained globally. Our study describes new phylogenetic species and the molecular characteristics of Histoplasma lineages causing outbreaks with a high number of severe outcomes in Northeast Brazil between 2011 and 2015. Genetic diversity levels provide evidence for recombination, common ancestry and clustering of Brazilian isolates at different geographic scales with the emergence of LAm C, a new genotype assigned to a separate population cluster in Northeast Brazil that exhibited low diversity indicative of isolation. The global survey revealed that the high genetic variability among Brazilian isolates along with the presence of divergent cryptic species and/or genotypes may support the hypothesis of Brazil being the center of dispersion of Histoplasma in South America, possibly with the contribution of migratory hosts such as birds and bats. Outside Brazil, the predominant species depends on the region. We confirm that histoplasmosis has significantly broadened its area of occurrence, an important feature of emerging pathogens. From a practical point of view, our data point to the emergence of histoplasmosis caused by a plethora of genotypes, and will enable epidemiological analysis focused on understanding the processes that lead to histoplasmosis. Further, the description of this diversity opens avenues for comparative genomic studies, which will allow progress toward a consensus taxonomy, improve understanding of the presence of hybrids in natural populations of medically relevant fungi, test reproductive barriers and to explore the significance of this variation. Key words: Emerging pathogens, Epidemiology, Genetic diversity, Histoplasma capsulatum, Histoplasmosis, Population structure. Published online xxx; https://doi.org/10.1016/j.simyco.2020.02.001. INTRODUCTION 0.1 to 1 case per 100 000 inhabitants per year in temperate climates, 10 to 100 cases per 100 000 in the humid tropics, and Histoplasmosis is a life-threatening systemic infection caused by over 100 cases per 100 000 in high risk groups and during the fungal pathogen Histoplasma capsulatum. This pathogen outbreaks (Colombo et al. 2011, Adenis et al. 2018). Although was first described in Panama in 1906 by Samuel T. Darling most infections are not outbreak-associated, outbreaks of his- (Darling 1906), followed shortly thereafter by reported infections toplasmosis linked to a common source do occasionally occur throughout the Americas (Riley & Watson 1926, Negroni 1940, and often involve activities that disrupt soil, especially samples Furcow 1958) and later in widely scattered places around the that contains bird or bat droppings (Queiroz-Telles et al. 2017). world (Rocher 1950, Ashbee et al. 2008, Antinori 2014, Baker Mammals become infected after inhaling Histoplasma prop- et al. 2019). The first epidemiological investigations in the mid- agules from the environment (Deepe 2018), which leads, in the 1940s revealed that Darling’s disease was more frequent than vast majority of human cases, to a primary pulmonary infection previously thought (Christie & Peterson 1945). There is an that is unapparent, subclinical or completely benign (Eissenberg increasing awareness of histoplasmosis in Central and South & Goldman 1991). The remaining patients may develop chronic America in patients with HIV/AIDS, and deaths from histoplas- progressive lung disease, chronic cutaneous or systemic dis- mosis in this region may outnumber deaths from tuberculosis ease, or an acute fulminating, rapidly fatal, systemic infection (Pasqualotto & Queiroz-Telles 2018, Linder & Kauffman 2019, (Kauffman 2007, Oladele et al. 2018). The infection is also very Nacher et al. 2019). Currently, histoplasmosis is one of the common in wild (e.g., marsupials, rodents, armadillos, sloths, world’s leading systemic infections, with incidence ranging from bats) and domestic animals (e.g., dogs and cats) in endemic Studies in Mycology Peer review under responsibility of Westerdijk Fungal Biodiversity Institute. © 2020 Westerdijk Fungal Biodiversity Institute. Production and hosting by ELSEVIER B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). 1 RODRIGUES ET AL. areas (Emmons 1950, Seyedmousavi et al. 2018). However, presentations needs to be confirmed in a large group of patients. mammals appear to be dead-end hosts of Histoplasma since Previous studies indicate that H. suramericanum causes an there is no person-to-person or animal-to-person spread. acute pulmonary disease with a pronounced lung pathology that For over a century histoplasmosis was attributed to a single leads to high mortality, whereas H. mississippiense and etiological agent, H. capsulatum (Onygenales). Judging from H. ohiense cause a chronic pulmonary disease (Durkin et al. different clinical manifestations, morphologies and wide-ranging 2004, Sepúlveda et al. 2017). H. capsulatum var. duboisii was geographical occurrence, three different varieties are historical- recently associated with AIDS and disseminated disease and to ly recognised: (i) H. capsulatum var. capsulatum, which is a a lesser extent with skin lesions in immunocompetent persons broadly dispersed New World human pathogen, responsible for (Oladele et al. 2018, Valero et al. 2018). classic histoplasmosis (Eissenberg & Goldman 1991); (ii) Several studies at the molecular level have been conducted H. capsulatum var. duboisii, a human pathogen confined to to elucidate the genetic diversity and population structure of Central and West Africa, causing African histoplasmosis, whose Histoplasma using molecular markers, ranging from DNA principal features are skin or bone lesions (Loulergue et al. 2007, sequencing to DNA fingerprinting (Damasceno et al. 2016, Pakasa et al. 2018); and (iii) H. capsulatum var. farciminosum,an Sahaza et al. 2019). In Brazil, high genetic diversity correlates Old World animal pathogen, responsible for epizootic lym- with the geographical origin (Zancope-Oliveira et al. 2005, Muniz phangitis in equines (Selim et al. 1985). Mde et al. 2010, Almeida et al. 2019). However, the origin of the Previous studies exploring phylogeography, gene flow and Brazilian Histoplasma populations and their relationship with the hybridisation processes have shown that the causal agents of global populations remain unknown, especially considering the histoplasmosis encompass several cryptic species, which are recently proposed taxonomic changes. Hence, the aims of the structured according to their geographical origin (Van Dyke et al. present study were to understand the genetic diversity of His- 2019). Kasuga and colleagues studied 137 isolates recovered toplasma isolates in Brazil and explore their evolutionary re- from 25 countries on six continents and were able to recognise at lationships with H. capsulatum s. str., H. capsulatum var. duboisii, least eight clades within seven phylogenetic species, including: H. suramericanum, H. mississippiense and H. ohiense. We used (i) North American class 1 clade (NAm 1); (ii) North American multi-locus sequence data from protein coding loci (ADP-ribo- class 2 clade (NAm 2); (iii) Latin American
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