Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses
ABSTRACT Mycoviruses are widespread and purportedly common throughout the fungal kingdom, although most are known from hosts in the two most recently diverged phyla, Ascomycota and Basidiomycota, together called Dikarya. To augment our knowledge of mycovirus prevalence and diversity in underexplored...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-10-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02027-20 |
| _version_ | 1818837735686799360 |
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| author | J. M. Myers A. E. Bonds R. A. Clemons N. A. Thapa D. R. Simmons D. Carter-House J. Ortanez P. Liu A. Miralles-Durán A. Desirò J. E. Longcore G. Bonito J. E. Stajich J. W. Spatafora Y. Chang L. M. Corrochano A. Gryganskyi I. V. Grigoriev T. Y. James |
| author_facet | J. M. Myers A. E. Bonds R. A. Clemons N. A. Thapa D. R. Simmons D. Carter-House J. Ortanez P. Liu A. Miralles-Durán A. Desirò J. E. Longcore G. Bonito J. E. Stajich J. W. Spatafora Y. Chang L. M. Corrochano A. Gryganskyi I. V. Grigoriev T. Y. James |
| author_sort | J. M. Myers |
| collection | DOAJ |
| description | ABSTRACT Mycoviruses are widespread and purportedly common throughout the fungal kingdom, although most are known from hosts in the two most recently diverged phyla, Ascomycota and Basidiomycota, together called Dikarya. To augment our knowledge of mycovirus prevalence and diversity in underexplored fungi, we conducted a large-scale survey of fungi in the earlier-diverging lineages, using both culture-based and transcriptome-mining approaches to search for RNA viruses. In total, 21.6% of 333 isolates were positive for RNA mycoviruses. This is a greater proportion than expected based on previous taxonomically broad mycovirus surveys and is suggestive of a strong phylogenetic component to mycoviral infection. Our newly found viral sequences are diverse, composed of double-stranded RNA, positive-sense single-stranded RNA (ssRNA), and negative-sense ssRNA genomes and include novel lineages lacking representation in the public databases. These identified viruses could be classified into 2 orders, 5 families, and 5 genera; however, half of the viruses remain taxonomically unassigned. Further, we identified a lineage of virus-like sequences in the genomes of members of Phycomycetaceae and Mortierellales that appear to be novel genes derived from integration of a viral RNA-dependent RNA polymerase gene. The two screening methods largely agreed in their detection of viruses; thus, we suggest that the culture-based assay is a cost-effective means to quickly assess whether a laboratory culture is virally infected. This study used culture collections and publicly available transcriptomes to demonstrate that mycoviruses are abundant in laboratory cultures of early-diverging fungal lineages. The function and diversity of mycoviruses found here will help guide future studies into mycovirus origins and ecological functions. IMPORTANCE Viruses are key drivers of evolution and ecosystem function and are increasingly recognized as symbionts of fungi. Fungi in early-diverging lineages are widespread, ecologically important, and comprise the majority of the phylogenetic diversity of the kingdom. Viruses infecting early-diverging lineages of fungi have been almost entirely unstudied. In this study, we screened fungi for viruses by two alternative approaches: a classic culture-based method and by transcriptome-mining. The results of our large-scale survey demonstrate that early-diverging lineages have higher infection rates than have been previously reported in other fungal taxa and that laboratory strains worldwide are host to infections, the implications of which are unknown. The function and diversity of mycoviruses found in these basal fungal lineages will help guide future studies into mycovirus origins and their evolutionary ramifications and ecological impacts. |
| first_indexed | 2024-12-19T03:27:14Z |
| format | Article |
| id | doaj.art-525a65541c234a629457332aa86469cb |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T03:27:14Z |
| publishDate | 2020-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-525a65541c234a629457332aa86469cb2022-12-21T20:37:35ZengAmerican Society for MicrobiologymBio2150-75112020-10-0111510.1128/mBio.02027-20Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse MycovirusesJ. M. Myers0A. E. Bonds1R. A. Clemons2N. A. Thapa3D. R. Simmons4D. Carter-House5J. Ortanez6P. Liu7A. Miralles-Durán8A. Desirò9J. E. Longcore10G. Bonito11J. E. Stajich12J. W. Spatafora13Y. Chang14L. M. Corrochano15A. Gryganskyi16I. V. Grigoriev17T. Y. James18University of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAUniversity of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAUniversity of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAUniversity of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAUniversity of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAUniversity of California—Riverside, Department of Microbiology and Plant Pathology, Riverside, California, USAUniversity of California—Riverside, Department of Microbiology and Plant Pathology, Riverside, California, USAUniversity of California—Riverside, Department of Microbiology and Plant Pathology, Riverside, California, USAUniversity of Seville, Department of Genetics, Seville, SpainMichigan State University, Department of Plant Soil and Microbial Sciences, East Lansing, Michigan, USAUniversity of Maine, School of Biology and Ecology, Orono, Maine, USAMichigan State University, Department of Plant Soil and Microbial Sciences, East Lansing, Michigan, USAUniversity of California—Riverside, Department of Microbiology and Plant Pathology, Riverside, California, USAOregon State University, Department of Botany and Plant Pathology, Corvalis, Oregon, USAOregon State University, Department of Botany and Plant Pathology, Corvalis, Oregon, USAUniversity of Seville, Department of Genetics, Seville, SpainL. F. Lambert Spawn Co., Coatesville, Pennsylvania, USAU.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USAUniversity of Michigan, Department of Ecology and Evolutionary Biology, Ann Arbor, Michigan, USAABSTRACT Mycoviruses are widespread and purportedly common throughout the fungal kingdom, although most are known from hosts in the two most recently diverged phyla, Ascomycota and Basidiomycota, together called Dikarya. To augment our knowledge of mycovirus prevalence and diversity in underexplored fungi, we conducted a large-scale survey of fungi in the earlier-diverging lineages, using both culture-based and transcriptome-mining approaches to search for RNA viruses. In total, 21.6% of 333 isolates were positive for RNA mycoviruses. This is a greater proportion than expected based on previous taxonomically broad mycovirus surveys and is suggestive of a strong phylogenetic component to mycoviral infection. Our newly found viral sequences are diverse, composed of double-stranded RNA, positive-sense single-stranded RNA (ssRNA), and negative-sense ssRNA genomes and include novel lineages lacking representation in the public databases. These identified viruses could be classified into 2 orders, 5 families, and 5 genera; however, half of the viruses remain taxonomically unassigned. Further, we identified a lineage of virus-like sequences in the genomes of members of Phycomycetaceae and Mortierellales that appear to be novel genes derived from integration of a viral RNA-dependent RNA polymerase gene. The two screening methods largely agreed in their detection of viruses; thus, we suggest that the culture-based assay is a cost-effective means to quickly assess whether a laboratory culture is virally infected. This study used culture collections and publicly available transcriptomes to demonstrate that mycoviruses are abundant in laboratory cultures of early-diverging fungal lineages. The function and diversity of mycoviruses found here will help guide future studies into mycovirus origins and ecological functions. IMPORTANCE Viruses are key drivers of evolution and ecosystem function and are increasingly recognized as symbionts of fungi. Fungi in early-diverging lineages are widespread, ecologically important, and comprise the majority of the phylogenetic diversity of the kingdom. Viruses infecting early-diverging lineages of fungi have been almost entirely unstudied. In this study, we screened fungi for viruses by two alternative approaches: a classic culture-based method and by transcriptome-mining. The results of our large-scale survey demonstrate that early-diverging lineages have higher infection rates than have been previously reported in other fungal taxa and that laboratory strains worldwide are host to infections, the implications of which are unknown. The function and diversity of mycoviruses found in these basal fungal lineages will help guide future studies into mycovirus origins and their evolutionary ramifications and ecological impacts.https://journals.asm.org/doi/10.1128/mBio.02027-20mycovirusdsRNA virusChytridiomycotaBlastocladiomycotaNeocallimastigomycotaZoopagomycota |
| spellingShingle | J. M. Myers A. E. Bonds R. A. Clemons N. A. Thapa D. R. Simmons D. Carter-House J. Ortanez P. Liu A. Miralles-Durán A. Desirò J. E. Longcore G. Bonito J. E. Stajich J. W. Spatafora Y. Chang L. M. Corrochano A. Gryganskyi I. V. Grigoriev T. Y. James Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses mBio mycovirus dsRNA virus Chytridiomycota Blastocladiomycota Neocallimastigomycota Zoopagomycota |
| title | Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses |
| title_full | Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses |
| title_fullStr | Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses |
| title_full_unstemmed | Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses |
| title_short | Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses |
| title_sort | survey of early diverging lineages of fungi reveals abundant and diverse mycoviruses |
| topic | mycovirus dsRNA virus Chytridiomycota Blastocladiomycota Neocallimastigomycota Zoopagomycota |
| url | https://journals.asm.org/doi/10.1128/mBio.02027-20 |
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