Pathogenic Allodiploid Hybrids of Aspergillus Fungi

Jacob L Steenwyk; Abigail L Lind; Laure N A Ries; Thaila F Dos Reis; Lilian P Silva; Fausto Almeida; Rafael W Bastos; Thais Fernanda de Campos Fraga da Silva; Vania L D Bonato; André Moreira Pessoni; Fernando Rodrigues; Huzefa A Raja; Sonja L Knowles; Nicholas H Oberlies; Katrien Lagrou; Gustavo H Goldman; Antonis Rokas

doi:10.1016/j.cub.2020.04.071

Pathogenic Allodiploid Hybrids of Aspergillus Fungi

Curr Biol. 2020 Jul 6;30(13):2495-2507.e7. doi: 10.1016/j.cub.2020.04.071. Epub 2020 Jun 4.

Authors

Jacob L Steenwyk¹, Abigail L Lind², Laure N A Ries³, Thaila F Dos Reis³, Lilian P Silva⁴, Fausto Almeida⁵, Rafael W Bastos⁴, Thais Fernanda de Campos Fraga da Silva⁵, Vania L D Bonato⁵, André Moreira Pessoni⁵, Fernando Rodrigues⁶, Huzefa A Raja⁷, Sonja L Knowles⁷, Nicholas H Oberlies⁷, Katrien Lagrou⁸, Gustavo H Goldman⁹, Antonis Rokas¹⁰

Affiliations

¹ Department of Biological Sciences, Vanderbilt University, 465 21st Avenue South, Nashville, TN 37235, USA.
² Department of Biomedical Informatics, Vanderbilt University School of Medicine, 1211 Medical Center Drive, Nashville, TN 37232, USA; Gladstone Institute of Data Science and Biotechnology, San Francisco, CA 94158, USA.
³ Departamento de Bioquímica e Imunologia, Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FMRP-USP), Avenida Bandeirantes 3900, Vila Monte Alegre, 14049-900 Ribeirão Preto, São Paulo, Brazil; Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, Avenida do Café S/N, Ribeirão Preto 14040-903, Brazil.
⁴ Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, Avenida do Café S/N, Ribeirão Preto 14040-903, Brazil.
⁵ Departamento de Bioquímica e Imunologia, Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo (FMRP-USP), Avenida Bandeirantes 3900, Vila Monte Alegre, 14049-900 Ribeirão Preto, São Paulo, Brazil.
⁶ Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, 4715-495 Braga, Portugal; ICVS/3B's-PT Government Associate Laboratory, 4715-495 Braga, Portugal.
⁷ Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, 1400 Spring Garden Street, Greensboro, NC 27412, USA.
⁸ Department of Microbiology, Immunology and Transplantation, Katholieke Universiteit Leuven, 3000 Leuven, Belgium; Department of Laboratory Medicine and National Reference Centre for Mycosis, University Hospitals Leuven, 3000 Leuven, Belgium.
⁹ Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, Avenida do Café S/N, Ribeirão Preto 14040-903, Brazil. Electronic address: [email protected].
¹⁰ Department of Biological Sciences, Vanderbilt University, 465 21st Avenue South, Nashville, TN 37235, USA; Department of Biomedical Informatics, Vanderbilt University School of Medicine, 1211 Medical Center Drive, Nashville, TN 37232, USA. Electronic address: [email protected].

Abstract

Interspecific hybridization substantially alters genotypes and phenotypes and can give rise to new lineages. Hybrid isolates that differ from their parental species in infection-relevant traits have been observed in several human-pathogenic yeasts and plant-pathogenic filamentous fungi but have yet to be found in human-pathogenic filamentous fungi. We discovered 6 clinical isolates from patients with aspergillosis originally identified as Aspergillus nidulans (section Nidulantes) that are actually allodiploid hybrids formed by the fusion of Aspergillus spinulosporus with an unknown close relative of Aspergillus quadrilineatus, both in section Nidulantes. Evolutionary genomic analyses revealed that these isolates belong to Aspergillus latus, an allodiploid hybrid species. Characterization of diverse infection-relevant traits further showed that A. latus hybrid isolates are genomically and phenotypically heterogeneous but also differ from A. nidulans, A. spinulosporus, and A. quadrilineatus. These results suggest that allodiploid hybridization contributes to the genomic and phenotypic diversity of filamentous fungal pathogens of humans.

Keywords: Eurotiomycetes; allopolyploidy; ascomycota; aspergillosis; cryptic species; fungal pathogen evolution; hybridization; nonvertical evolution; pathogenicity; virulence.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Aspergillus / genetics*
Aspergillus / isolation & purification
Diploidy
Genome, Fungal*
Genomics
Hybridization, Genetic*

Supplementary concepts

Aspergillus latus
Aspergillus quadrilineatus
Aspergillus spinulosporus

Abstract

Publication types

MeSH terms

Supplementary concepts

Grants and funding