ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations
ABSTRACT Ostreid herpesvirus-1 (OsHV-1) RNAs are enzymatically modified by A-to-I conversions during the infection of Crassostrea gigas. The increase of ADAR1 expression and hyper-editing activity parallel to OsHV-1 RNAs suggests a functional connection between dsRNA editing and antiviral responses....
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Format: | Article |
Language: | English |
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American Society for Microbiology
2022-04-01
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Series: | mSphere |
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Online Access: | https://journals.asm.org/doi/10.1128/msphere.00011-22 |
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author | Umberto Rosani Enrico Bortoletto Caroline Montagnani Paola Venier |
author_facet | Umberto Rosani Enrico Bortoletto Caroline Montagnani Paola Venier |
author_sort | Umberto Rosani |
collection | DOAJ |
description | ABSTRACT Ostreid herpesvirus-1 (OsHV-1) RNAs are enzymatically modified by A-to-I conversions during the infection of Crassostrea gigas. The increase of ADAR1 expression and hyper-editing activity parallel to OsHV-1 RNAs suggests a functional connection between dsRNA editing and antiviral responses. We analyzed 87 RNA-seq data sets from immuno-primed, resistant, and susceptible oysters exposed to OsHV-1 to compare the ADAR hyper-editing levels on host and viral transcripts and trace hyper-editing on the oyster genes. Host RNAs were more hyper-edited than viral RNAs, despite the increased editing of viral RNAs in late infection phases. A set of genes, representing ∼0.5% of the oyster transcriptome and including several tripartite motif-containing sequences, were constantly hyper-edited. Conversely, we identified genes involved in antiviral response, miRNA maturation, and epigenetic regulation that were hyper-edited in specific conditions only. Despite technical and biological bottlenecks that hamper the understanding of the bivalve “RNA editome,” available tools and technologies can be adapted to bivalve mollusks. IMPORTANCE Ostreid herpesvirus-1 (OsHV-1) is a harmful pathogen of bivalve species, such as oysters. However, knowledge is lacking about host–virus interactions at the molecular level, hampering the possibility of a correct management of viral outbreaks and related massive mortalities. Notably, OsHV-1 transcripts are massively modified by host RNA editing enzyme during infection, resulting in multiple A-to-I variations along RNAs assuming double-strand conformations. The impact of these modifications on host transcripts is, however, not completely clear. Analyzing RNA-seq data of oysters infected with OsHV-1, we revealed that ∼0.5% of the oyster transcriptome is always enzymatically modified by ADAR, whereas genes involved in antiviral response, miRNA maturation, and epigenetic regulation were hyper-edited in specific conditions only. Despite our results, relevant technical bottlenecks impair an accurate quantification of RNA editing events, making necessary an approach specifically dedicated to the progressive understanding of oyster “RNA editome.” |
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format | Article |
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institution | Directory Open Access Journal |
issn | 2379-5042 |
language | English |
last_indexed | 2024-04-13T22:40:35Z |
publishDate | 2022-04-01 |
publisher | American Society for Microbiology |
record_format | Article |
series | mSphere |
spelling | doaj.art-08a0d63299d5444dbcebb78826bb8f512022-12-22T02:26:38ZengAmerican Society for MicrobiologymSphere2379-50422022-04-017210.1128/msphere.00011-22ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and LimitationsUmberto Rosani0Enrico Bortoletto1Caroline Montagnani2Paola Venier3Department of Biology, University of Padova, Padova, ItalyDepartment of Biology, University of Padova, Padova, ItalyIHPE, CNRS, Ifremer, Université Montpellier, Montpellier, FranceDepartment of Biology, University of Padova, Padova, ItalyABSTRACT Ostreid herpesvirus-1 (OsHV-1) RNAs are enzymatically modified by A-to-I conversions during the infection of Crassostrea gigas. The increase of ADAR1 expression and hyper-editing activity parallel to OsHV-1 RNAs suggests a functional connection between dsRNA editing and antiviral responses. We analyzed 87 RNA-seq data sets from immuno-primed, resistant, and susceptible oysters exposed to OsHV-1 to compare the ADAR hyper-editing levels on host and viral transcripts and trace hyper-editing on the oyster genes. Host RNAs were more hyper-edited than viral RNAs, despite the increased editing of viral RNAs in late infection phases. A set of genes, representing ∼0.5% of the oyster transcriptome and including several tripartite motif-containing sequences, were constantly hyper-edited. Conversely, we identified genes involved in antiviral response, miRNA maturation, and epigenetic regulation that were hyper-edited in specific conditions only. Despite technical and biological bottlenecks that hamper the understanding of the bivalve “RNA editome,” available tools and technologies can be adapted to bivalve mollusks. IMPORTANCE Ostreid herpesvirus-1 (OsHV-1) is a harmful pathogen of bivalve species, such as oysters. However, knowledge is lacking about host–virus interactions at the molecular level, hampering the possibility of a correct management of viral outbreaks and related massive mortalities. Notably, OsHV-1 transcripts are massively modified by host RNA editing enzyme during infection, resulting in multiple A-to-I variations along RNAs assuming double-strand conformations. The impact of these modifications on host transcripts is, however, not completely clear. Analyzing RNA-seq data of oysters infected with OsHV-1, we revealed that ∼0.5% of the oyster transcriptome is always enzymatically modified by ADAR, whereas genes involved in antiviral response, miRNA maturation, and epigenetic regulation were hyper-edited in specific conditions only. Despite our results, relevant technical bottlenecks impair an accurate quantification of RNA editing events, making necessary an approach specifically dedicated to the progressive understanding of oyster “RNA editome.”https://journals.asm.org/doi/10.1128/msphere.00011-22ADAR1hyper-editingoysterOsHV-1antiviral immunityADAR |
spellingShingle | Umberto Rosani Enrico Bortoletto Caroline Montagnani Paola Venier ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations mSphere ADAR1 hyper-editing oyster OsHV-1 antiviral immunity ADAR |
title | ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations |
title_full | ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations |
title_fullStr | ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations |
title_full_unstemmed | ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations |
title_short | ADAR-Editing during Ostreid Herpesvirus 1 Infection in Crassostrea gigas: Facts and Limitations |
title_sort | adar editing during ostreid herpesvirus 1 infection in crassostrea gigas facts and limitations |
topic | ADAR1 hyper-editing oyster OsHV-1 antiviral immunity ADAR |
url | https://journals.asm.org/doi/10.1128/msphere.00011-22 |
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