Tracing histoplasmosis genomic epidemiology and species occurrence across the USA

Histoplasmosis is an endemic mycosis in North America frequently reported along the Ohio and Mississippi River Valleys, although autochthonous cases occur in non-endemic areas. In the United States, the disease is provoked by two genetically distinct clades of Histoplasma capsulatum sensu lato, Hist...

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Main Authors: Bernardo Guerra Tenório, Daniel R. Kollath, Lalitha Gade, Anastasia P. Litvintseva, Tom Chiller, Jeff S. Jenness, Jason E. Stajich, Daniel R. Matute, Andrew S. Hanzlicek, Bridget M. Barker, Marcus de Melo Teixeira
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2024.2315960
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author Bernardo Guerra Tenório
Daniel R. Kollath
Lalitha Gade
Anastasia P. Litvintseva
Tom Chiller
Jeff S. Jenness
Jason E. Stajich
Daniel R. Matute
Andrew S. Hanzlicek
Bridget M. Barker
Marcus de Melo Teixeira
author_facet Bernardo Guerra Tenório
Daniel R. Kollath
Lalitha Gade
Anastasia P. Litvintseva
Tom Chiller
Jeff S. Jenness
Jason E. Stajich
Daniel R. Matute
Andrew S. Hanzlicek
Bridget M. Barker
Marcus de Melo Teixeira
author_sort Bernardo Guerra Tenório
collection DOAJ
description Histoplasmosis is an endemic mycosis in North America frequently reported along the Ohio and Mississippi River Valleys, although autochthonous cases occur in non-endemic areas. In the United States, the disease is provoked by two genetically distinct clades of Histoplasma capsulatum sensu lato, Histoplasma mississippiense (Nam1) and H. ohiense (Nam2). To bridge the molecular epidemiological gap, we genotyped 93 Histoplasma isolates (62 novel genomes) including clinical, environmental, and veterinarian samples from a broader geographical range by whole-genome sequencing, followed by evolutionary and species niche modelling analyses. We show that histoplasmosis is caused by two major lineages, H. ohiense and H. mississippiense; with sporadic cases caused by H. suramericanum in California and Texas. While H. ohiense is prevalent in eastern states, H. mississipiense was found to be prevalent in the central and western portions of the United States, but also geographically overlapping in some areas suggesting that these species might co-occur. Species Niche Modelling revealed that H. ohiense thrives in places with warmer and drier conditions, while H. mississippiense is endemic to areas with cooler temperatures and more precipitation. In addition, we predicted multiple areas of secondary contact zones where the two species co-occur, potentially facilitating gene exchange and hybridization. This study provides the most comprehensive understanding of the genomic epidemiology of histoplasmosis in the USA and lays a blueprint for the study of invasive fungal diseases.
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spelling doaj-art-ca2000f8172542a2aa0c068e90e1e4732025-08-20T02:37:32ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512024-12-0113110.1080/22221751.2024.2315960Tracing histoplasmosis genomic epidemiology and species occurrence across the USABernardo Guerra Tenório0Daniel R. Kollath1Lalitha Gade2Anastasia P. Litvintseva3Tom Chiller4Jeff S. Jenness5Jason E. Stajich6Daniel R. Matute7Andrew S. Hanzlicek8Bridget M. Barker9Marcus de Melo Teixeira10Faculty of Medicine, University of Brasília, Brasília, BrazilPathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, USAMycotic Diseases Branch, Centers for Disease Control and Prevention, Atlanta, GA, USAMycotic Diseases Branch, Centers for Disease Control and Prevention, Atlanta, GA, USAMycotic Diseases Branch, Centers for Disease Control and Prevention, Atlanta, GA, USASchool of Forestry, Northern Arizona University, Flagstaff, AZ, USADepartment of Microbiology & Plant Pathology and Institute for Integrative Genome Biology, University of California, Riverside, CA, USABiology Department, University of North Carolina, Chapel Hill, NC, USAMiraVista Diagnostics, Indianapolis, IN, USAPathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, USAFaculty of Medicine, University of Brasília, Brasília, BrazilHistoplasmosis is an endemic mycosis in North America frequently reported along the Ohio and Mississippi River Valleys, although autochthonous cases occur in non-endemic areas. In the United States, the disease is provoked by two genetically distinct clades of Histoplasma capsulatum sensu lato, Histoplasma mississippiense (Nam1) and H. ohiense (Nam2). To bridge the molecular epidemiological gap, we genotyped 93 Histoplasma isolates (62 novel genomes) including clinical, environmental, and veterinarian samples from a broader geographical range by whole-genome sequencing, followed by evolutionary and species niche modelling analyses. We show that histoplasmosis is caused by two major lineages, H. ohiense and H. mississippiense; with sporadic cases caused by H. suramericanum in California and Texas. While H. ohiense is prevalent in eastern states, H. mississipiense was found to be prevalent in the central and western portions of the United States, but also geographically overlapping in some areas suggesting that these species might co-occur. Species Niche Modelling revealed that H. ohiense thrives in places with warmer and drier conditions, while H. mississippiense is endemic to areas with cooler temperatures and more precipitation. In addition, we predicted multiple areas of secondary contact zones where the two species co-occur, potentially facilitating gene exchange and hybridization. This study provides the most comprehensive understanding of the genomic epidemiology of histoplasmosis in the USA and lays a blueprint for the study of invasive fungal diseases.https://www.tandfonline.com/doi/10.1080/22221751.2024.2315960Histoplasmosismolecular epidemiologyHistoplasma ohienseHistoplasma mississippiensegenomicsspecies distribution modelling
spellingShingle Bernardo Guerra Tenório
Daniel R. Kollath
Lalitha Gade
Anastasia P. Litvintseva
Tom Chiller
Jeff S. Jenness
Jason E. Stajich
Daniel R. Matute
Andrew S. Hanzlicek
Bridget M. Barker
Marcus de Melo Teixeira
Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
Emerging Microbes and Infections
Histoplasmosis
molecular epidemiology
Histoplasma ohiense
Histoplasma mississippiense
genomics
species distribution modelling
title Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
title_full Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
title_fullStr Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
title_full_unstemmed Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
title_short Tracing histoplasmosis genomic epidemiology and species occurrence across the USA
title_sort tracing histoplasmosis genomic epidemiology and species occurrence across the usa
topic Histoplasmosis
molecular epidemiology
Histoplasma ohiense
Histoplasma mississippiense
genomics
species distribution modelling
url https://www.tandfonline.com/doi/10.1080/22221751.2024.2315960
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