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Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort

Emerging infections caused by fungi have become a widely recognized global phenomenon and are causing an increasing burden of disease. Genomic techniques are providing new insights into the structure of fungal populations, revealing hitherto undescribed fine‐scale adaptations to environments and hos...

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Autores principales: Vanhove, Mathieu, Beale, Mathew A., Rhodes, Johanna, Chanda, Duncan, Lakhi, Shabir, Kwenda, Geoffrey, Molloy, Sile, Karunaharan, Natasha, Stone, Neil, Harrison, Thomas S., Bicanic, Tihana, Fisher, Matthew C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5412878/
https://www.ncbi.nlm.nih.gov/pubmed/27862555
http://dx.doi.org/10.1111/mec.13891
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author Vanhove, Mathieu
Beale, Mathew A.
Rhodes, Johanna
Chanda, Duncan
Lakhi, Shabir
Kwenda, Geoffrey
Molloy, Sile
Karunaharan, Natasha
Stone, Neil
Harrison, Thomas S.
Bicanic, Tihana
Fisher, Matthew C.
author_facet Vanhove, Mathieu
Beale, Mathew A.
Rhodes, Johanna
Chanda, Duncan
Lakhi, Shabir
Kwenda, Geoffrey
Molloy, Sile
Karunaharan, Natasha
Stone, Neil
Harrison, Thomas S.
Bicanic, Tihana
Fisher, Matthew C.
author_sort Vanhove, Mathieu
collection PubMed
description Emerging infections caused by fungi have become a widely recognized global phenomenon and are causing an increasing burden of disease. Genomic techniques are providing new insights into the structure of fungal populations, revealing hitherto undescribed fine‐scale adaptations to environments and hosts that govern their emergence as infections. Cryptococcal meningitis is a neglected tropical disease that is responsible for a large proportion of AIDS‐related deaths across Africa; however, the ecological determinants that underlie a patient's risk of infection remain largely unexplored. Here, we use genome sequencing and ecological genomics to decipher the evolutionary ecology of the aetiological agents of cryptococcal meningitis, Cryptococcus neoformans and Cryptococcus gattii, across the central African country of Zambia. We show that the occurrence of these two pathogens is differentially associated with biotic (macroecological) and abiotic (physical) factors across two key African ecoregions, Central Miombo woodlands and Zambezi Mopane woodlands. We show that speciation of Cryptococcus has resulted in adaptation to occupy different ecological niches, with C. neoformans found to occupy Zambezi Mopane woodlands and C. gattii primarily recovered from Central Miombo woodlands. Genome sequencing shows that C. neoformans causes 95% of human infections in this region, of which over three‐quarters belonged to the globalized lineage VNI. We show that VNI infections are largely associated with urbanized populations in Zambia. Conversely, the majority of C. neoformans isolates recovered in the environment belong to the genetically diverse African‐endemic lineage VNB, and we show hitherto unmapped levels of genomic diversity within this lineage. Our results reveal the complex evolutionary ecology that underpins the reservoirs of infection for this, and likely other, deadly pathogenic fungi.
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spelling pubmed-54128782017-05-15 Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort Vanhove, Mathieu Beale, Mathew A. Rhodes, Johanna Chanda, Duncan Lakhi, Shabir Kwenda, Geoffrey Molloy, Sile Karunaharan, Natasha Stone, Neil Harrison, Thomas S. Bicanic, Tihana Fisher, Matthew C. Mol Ecol Insights on Microbial Adaptation from Patterns of Local Adaptation in Nature Emerging infections caused by fungi have become a widely recognized global phenomenon and are causing an increasing burden of disease. Genomic techniques are providing new insights into the structure of fungal populations, revealing hitherto undescribed fine‐scale adaptations to environments and hosts that govern their emergence as infections. Cryptococcal meningitis is a neglected tropical disease that is responsible for a large proportion of AIDS‐related deaths across Africa; however, the ecological determinants that underlie a patient's risk of infection remain largely unexplored. Here, we use genome sequencing and ecological genomics to decipher the evolutionary ecology of the aetiological agents of cryptococcal meningitis, Cryptococcus neoformans and Cryptococcus gattii, across the central African country of Zambia. We show that the occurrence of these two pathogens is differentially associated with biotic (macroecological) and abiotic (physical) factors across two key African ecoregions, Central Miombo woodlands and Zambezi Mopane woodlands. We show that speciation of Cryptococcus has resulted in adaptation to occupy different ecological niches, with C. neoformans found to occupy Zambezi Mopane woodlands and C. gattii primarily recovered from Central Miombo woodlands. Genome sequencing shows that C. neoformans causes 95% of human infections in this region, of which over three‐quarters belonged to the globalized lineage VNI. We show that VNI infections are largely associated with urbanized populations in Zambia. Conversely, the majority of C. neoformans isolates recovered in the environment belong to the genetically diverse African‐endemic lineage VNB, and we show hitherto unmapped levels of genomic diversity within this lineage. Our results reveal the complex evolutionary ecology that underpins the reservoirs of infection for this, and likely other, deadly pathogenic fungi. John Wiley and Sons Inc. 2016-11-08 2017-04 /pmc/articles/PMC5412878/ /pubmed/27862555 http://dx.doi.org/10.1111/mec.13891 Text en © 2016 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Insights on Microbial Adaptation from Patterns of Local Adaptation in Nature
Vanhove, Mathieu
Beale, Mathew A.
Rhodes, Johanna
Chanda, Duncan
Lakhi, Shabir
Kwenda, Geoffrey
Molloy, Sile
Karunaharan, Natasha
Stone, Neil
Harrison, Thomas S.
Bicanic, Tihana
Fisher, Matthew C.
Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title_full Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title_fullStr Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title_full_unstemmed Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title_short Genomic epidemiology of Cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an African HIV/AIDS cohort
title_sort genomic epidemiology of cryptococcus yeasts identifies adaptation to environmental niches underpinning infection across an african hiv/aids cohort
topic Insights on Microbial Adaptation from Patterns of Local Adaptation in Nature
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5412878/
https://www.ncbi.nlm.nih.gov/pubmed/27862555
http://dx.doi.org/10.1111/mec.13891
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