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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-08-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00925-19 |
| _version_ | 1818407530789863424 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T09:29:18Z |
| format | Article |
| id | doaj.art-e321811240d9428a968d8200fff00ea4 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-14T09:29:18Z |
| publishDate | 2019-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-e321811240d9428a968d8200fff00ea42022-12-21T23:08:07ZengAmerican Society for MicrobiologymBio2150-75112019-08-0110410.1128/mBio.00925-19A Robust Phylogenomic Time Tree for Biotechnologically and Medically Important Fungi in the Genera <italic toggle="yes">Aspergillus</italic> and <italic toggle="yes">Penicillium</italic>Jacob L. Steenwyk0Xing-Xing Shen1Abigail L. Lind2Gustavo H. Goldman3Antonis Rokas4Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USADepartment of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USADepartment of Biomedical Informatics, Vanderbilt University School of Medicine, Nashville, Tennessee, USADepartamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Prêto, Universidade de São Paulo, São Paulo, BrazilDepartment of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.00925-19AscomycotaEurotialesEurotiomycetesgenomicsincongruenceInternational Code of Nomenclature |
| spellingShingle | 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> mBio Ascomycota Eurotiales Eurotiomycetes genomics incongruence International Code of Nomenclature |
| 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_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_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_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 |
| topic | Ascomycota Eurotiales Eurotiomycetes genomics incongruence International Code of Nomenclature |
| url | https://journals.asm.org/doi/10.1128/mBio.00925-19 |
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