A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>

ABSTRACT The filamentous fungal family Aspergillaceae contains >1,000 known species, mostly in the genera Aspergillus and Penicillium. Several species are used in the food, biotechnology, and drug industries (e.g., Aspergillus oryzae and Penicillium camemberti), while others are dangerous human a...

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Autores principales:	Jacob L. Steenwyk, Xing-Xing Shen, Abigail L. Lind, Gustavo H. Goldman, Antonis Rokas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Ascomycota Eurotiales Eurotiomycetes genomics incongruence International Code of Nomenclature Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e321811240d9428a968d8200fff00ea4
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spelling	oai:doaj.org-article:e321811240d9428a968d8200fff00ea42021-11-15T16:22:08ZA Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>10.1128/mBio.00925-192150-7511https://doaj.org/article/e321811240d9428a968d8200fff00ea42019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00925-19https://doaj.org/toc/2150-7511ABSTRACT The filamentous fungal family Aspergillaceae contains >1,000 known species, mostly in the genera Aspergillus and Penicillium. Several species are used in the food, biotechnology, and drug industries (e.g., Aspergillus oryzae and Penicillium camemberti), while others are dangerous human and plant pathogens (e.g., Aspergillus fumigatus and Penicillium digitatum). To infer a robust phylogeny and pinpoint poorly resolved branches and their likely underlying contributors, we used 81 genomes spanning the diversity of Aspergillus and Penicillium to construct a 1,668-gene data matrix. Phylogenies of the nucleotide and amino acid versions of this full data matrix as well as of several additional data matrices were generated using three different maximum likelihood schemes (i.e., gene-partitioned, unpartitioned, and coalescence) and using both site-homogenous and site-heterogeneous models (total of 64 species-level phylogenies). Examination of the topological agreement among these phylogenies and measures of internode certainty identified 11/78 (14.1%) bipartitions that were incongruent and pinpointed the likely underlying contributing factors, which included incomplete lineage sorting, hidden paralogy, hybridization or introgression, and reconstruction artifacts associated with poor taxon sampling. Relaxed molecular clock analyses suggest that Aspergillaceae likely originated in the lower Cretaceous and that the Aspergillus and Penicillium genera originated in the upper Cretaceous. Our results shed light on the ongoing debate on Aspergillus systematics and taxonomy and provide a robust evolutionary and temporal framework for comparative genomic analyses in Aspergillaceae. More broadly, our approach provides a general template for phylogenomic identification of resolved and contentious branches in densely genome-sequenced lineages across the tree of life. IMPORTANCE Understanding the evolution of traits across technologically and medically significant fungi requires a robust phylogeny. Even though species in the Aspergillus and Penicillium genera (family Aspergillaceae, class Eurotiomycetes) are some of the most significant technologically and medically relevant fungi, we still lack a genome-scale phylogeny of the lineage or knowledge of the parts of the phylogeny that exhibit conflict among analyses. Here, we used a phylogenomic approach to infer evolutionary relationships among 81 genomes that span the diversity of Aspergillus and Penicillium species, to identify conflicts in the phylogeny, and to determine the likely underlying factors of the observed conflicts. Using a data matrix comprised of 1,668 genes, we found that while most branches of the phylogeny of the Aspergillaceae are robustly supported and recovered irrespective of method of analysis, a few exhibit various degrees of conflict among our analyses. Further examination of the observed conflict revealed that it largely stems from incomplete lineage sorting and hybridization or introgression. Our analyses provide a robust and comprehensive evolutionary genomic roadmap for this important lineage, which will facilitate the examination of the diverse technologically and medically relevant traits of these fungi in an evolutionary context.Jacob L. SteenwykXing-Xing ShenAbigail L. LindGustavo H. GoldmanAntonis RokasAmerican Society for MicrobiologyarticleAscomycotaEurotialesEurotiomycetesgenomicsincongruenceInternational Code of NomenclatureMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Ascomycota Eurotiales Eurotiomycetes genomics incongruence International Code of Nomenclature Microbiology QR1-502
spellingShingle	Ascomycota Eurotiales Eurotiomycetes genomics incongruence International Code of Nomenclature Microbiology QR1-502 Jacob L. Steenwyk Xing-Xing Shen Abigail L. Lind Gustavo H. Goldman Antonis Rokas A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
description	ABSTRACT The filamentous fungal family Aspergillaceae contains >1,000 known species, mostly in the genera Aspergillus and Penicillium. Several species are used in the food, biotechnology, and drug industries (e.g., Aspergillus oryzae and Penicillium camemberti), while others are dangerous human and plant pathogens (e.g., Aspergillus fumigatus and Penicillium digitatum). To infer a robust phylogeny and pinpoint poorly resolved branches and their likely underlying contributors, we used 81 genomes spanning the diversity of Aspergillus and Penicillium to construct a 1,668-gene data matrix. Phylogenies of the nucleotide and amino acid versions of this full data matrix as well as of several additional data matrices were generated using three different maximum likelihood schemes (i.e., gene-partitioned, unpartitioned, and coalescence) and using both site-homogenous and site-heterogeneous models (total of 64 species-level phylogenies). Examination of the topological agreement among these phylogenies and measures of internode certainty identified 11/78 (14.1%) bipartitions that were incongruent and pinpointed the likely underlying contributing factors, which included incomplete lineage sorting, hidden paralogy, hybridization or introgression, and reconstruction artifacts associated with poor taxon sampling. Relaxed molecular clock analyses suggest that Aspergillaceae likely originated in the lower Cretaceous and that the Aspergillus and Penicillium genera originated in the upper Cretaceous. Our results shed light on the ongoing debate on Aspergillus systematics and taxonomy and provide a robust evolutionary and temporal framework for comparative genomic analyses in Aspergillaceae. More broadly, our approach provides a general template for phylogenomic identification of resolved and contentious branches in densely genome-sequenced lineages across the tree of life. IMPORTANCE Understanding the evolution of traits across technologically and medically significant fungi requires a robust phylogeny. Even though species in the Aspergillus and Penicillium genera (family Aspergillaceae, class Eurotiomycetes) are some of the most significant technologically and medically relevant fungi, we still lack a genome-scale phylogeny of the lineage or knowledge of the parts of the phylogeny that exhibit conflict among analyses. Here, we used a phylogenomic approach to infer evolutionary relationships among 81 genomes that span the diversity of Aspergillus and Penicillium species, to identify conflicts in the phylogeny, and to determine the likely underlying factors of the observed conflicts. Using a data matrix comprised of 1,668 genes, we found that while most branches of the phylogeny of the Aspergillaceae are robustly supported and recovered irrespective of method of analysis, a few exhibit various degrees of conflict among our analyses. Further examination of the observed conflict revealed that it largely stems from incomplete lineage sorting and hybridization or introgression. Our analyses provide a robust and comprehensive evolutionary genomic roadmap for this important lineage, which will facilitate the examination of the diverse technologically and medically relevant traits of these fungi in an evolutionary context.
format	article
author	Jacob L. Steenwyk Xing-Xing Shen Abigail L. Lind Gustavo H. Goldman Antonis Rokas
author_facet	Jacob L. Steenwyk Xing-Xing Shen Abigail L. Lind Gustavo H. Goldman Antonis Rokas
author_sort	Jacob L. Steenwyk
title	A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
title_short	A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
title_full	A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
title_fullStr	A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
title_full_unstemmed	A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>
title_sort	robust phylogenomic time tree for biotechnologically and medically important fungi in the genera <italic toggle="yes">aspergillus</italic> and <italic toggle="yes">penicillium</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/e321811240d9428a968d8200fff00ea4
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A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>

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