A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response

ABSTRACT Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of Malassezia species. Ma...

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Autores principales: Minji Park, Yong-Joon Cho, Donggyu Kim, Chul-Su Yang, Shi Mun Lee, Thomas L. Dawson, Satoshi Nakamizo, Kenji Kabashima, Yang Won Lee, Won Hee Jung
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:9fd61a773d114523969eaf8b3ddf53ff2021-11-15T16:19:07ZA Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response10.1128/mBio.01521-202150-7511https://doaj.org/article/9fd61a773d114523969eaf8b3ddf53ff2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01521-20https://doaj.org/toc/2150-7511ABSTRACT Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of Malassezia species. Malassezia is the most dominant fungal genus on the human skin surface, and species in this group are considered etiological factors of various skin diseases including dandruff, seborrheic dermatitis, and atopic dermatitis. We identified novel dsRNA segments, and our sequencing results revealed that the virus, named MrV40, belongs to the Totiviridae family and contains an additional satellite dsRNA segment encoding a novel protein. The transcriptome of virus-infected Malassezia restricta cells was compared to that of virus-cured cells, and the results showed that transcripts involved in ribosomal biosynthesis were downregulated and those involved in energy production and programmed cell death were upregulated. Moreover, transmission electron microscopy revealed significantly larger vacuoles in virus-infected M. restricta cells, indicating that MrV40 infection dramatically altered M. restricta physiology. Our analysis also revealed that viral nucleic acid from MrV40 induced a TLR3 (Toll-like receptor 3)-mediated inflammatory immune response in bone marrow-derived dendritic cells, suggesting that a viral element contributes to the pathogenicity of Malassezia. IMPORTANCE Malassezia is the most dominant fungal genus on the human skin surface and is associated with various skin diseases including dandruff and seborrheic dermatitis. Among Malassezia species, Malassezia restricta is the most widely observed species on the human skin. In the current study, we identified a novel dsRNA virus, named MrV40, in M. restricta and characterized the sequence and structure of the viral genome along with an independent satellite dsRNA viral segment. Moreover, expression of genes involved in ribosomal synthesis and programmed cell death was altered, indicating that virus infection affected the physiology of the fungal host cells. Our data also showed that the viral nucleic acid from MrV40 induces a TLR3-mediated inflammatory immune response in bone marrow-derived dendritic cells, indicating that a viral element likely contributes to the pathogenicity of Malassezia. This is the first study to identify and characterize a novel mycovirus in Malassezia.Minji ParkYong-Joon ChoDonggyu KimChul-Su YangShi Mun LeeThomas L. DawsonSatoshi NakamizoKenji KabashimaYang Won LeeWon Hee JungAmerican Society for MicrobiologyarticleMalasseziaMalassezia restrictamycovirusTLR3cytokinedouble-stranded RNA virusMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic Malassezia
Malassezia restricta
mycovirus
TLR3
cytokine
double-stranded RNA virus
Microbiology
QR1-502
spellingShingle Malassezia
Malassezia restricta
mycovirus
TLR3
cytokine
double-stranded RNA virus
Microbiology
QR1-502
Minji Park
Yong-Joon Cho
Donggyu Kim
Chul-Su Yang
Shi Mun Lee
Thomas L. Dawson
Satoshi Nakamizo
Kenji Kabashima
Yang Won Lee
Won Hee Jung
A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
description ABSTRACT Most fungal viruses have been identified in plant pathogens, whereas the presence of viral particles in human-pathogenic fungi is less well studied. In the present study, we observed extrachromosomal double-stranded RNA (dsRNA) segments in various clinical isolates of Malassezia species. Malassezia is the most dominant fungal genus on the human skin surface, and species in this group are considered etiological factors of various skin diseases including dandruff, seborrheic dermatitis, and atopic dermatitis. We identified novel dsRNA segments, and our sequencing results revealed that the virus, named MrV40, belongs to the Totiviridae family and contains an additional satellite dsRNA segment encoding a novel protein. The transcriptome of virus-infected Malassezia restricta cells was compared to that of virus-cured cells, and the results showed that transcripts involved in ribosomal biosynthesis were downregulated and those involved in energy production and programmed cell death were upregulated. Moreover, transmission electron microscopy revealed significantly larger vacuoles in virus-infected M. restricta cells, indicating that MrV40 infection dramatically altered M. restricta physiology. Our analysis also revealed that viral nucleic acid from MrV40 induced a TLR3 (Toll-like receptor 3)-mediated inflammatory immune response in bone marrow-derived dendritic cells, suggesting that a viral element contributes to the pathogenicity of Malassezia. IMPORTANCE Malassezia is the most dominant fungal genus on the human skin surface and is associated with various skin diseases including dandruff and seborrheic dermatitis. Among Malassezia species, Malassezia restricta is the most widely observed species on the human skin. In the current study, we identified a novel dsRNA virus, named MrV40, in M. restricta and characterized the sequence and structure of the viral genome along with an independent satellite dsRNA viral segment. Moreover, expression of genes involved in ribosomal synthesis and programmed cell death was altered, indicating that virus infection affected the physiology of the fungal host cells. Our data also showed that the viral nucleic acid from MrV40 induces a TLR3-mediated inflammatory immune response in bone marrow-derived dendritic cells, indicating that a viral element likely contributes to the pathogenicity of Malassezia. This is the first study to identify and characterize a novel mycovirus in Malassezia.
format article
author Minji Park
Yong-Joon Cho
Donggyu Kim
Chul-Su Yang
Shi Mun Lee
Thomas L. Dawson
Satoshi Nakamizo
Kenji Kabashima
Yang Won Lee
Won Hee Jung
author_facet Minji Park
Yong-Joon Cho
Donggyu Kim
Chul-Su Yang
Shi Mun Lee
Thomas L. Dawson
Satoshi Nakamizo
Kenji Kabashima
Yang Won Lee
Won Hee Jung
author_sort Minji Park
title A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
title_short A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
title_full A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
title_fullStr A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
title_full_unstemmed A Novel Virus Alters Gene Expression and Vacuolar Morphology in <italic toggle="yes">Malassezia</italic> Cells and Induces a TLR3-Mediated Inflammatory Immune Response
title_sort novel virus alters gene expression and vacuolar morphology in <italic toggle="yes">malassezia</italic> cells and induces a tlr3-mediated inflammatory immune response
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/9fd61a773d114523969eaf8b3ddf53ff
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