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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Main Authors: Umberto Rosani, Enrico Bortoletto, Caroline Montagnani, Paola Venier
Format: Article
Language:English
Published: American Society for Microbiology 2022-04-01
Series:mSphere
Subjects:
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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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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