Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing
The highly versatile group of Herpesviruses cause disease in a wide range of hosts. In invertebrates, only two herpesviruses are known: the malacoherpesviruses HaHV-1 and OsHV-1 infecting gastropods and bivalves, respectively. To understand viral transcript architecture and diversity we first recons...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-09-01
|
| Series: | Viruses |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1999-4915/13/10/1971 |
| _version_ | 1797512983615635456 |
|---|---|
| author | Chang-Ming Bai Umberto Rosani Xiang Zhang Lu-Sheng Xin Enrico Bortoletto K. Mathias Wegner Chong-Ming Wang |
| author_facet | Chang-Ming Bai Umberto Rosani Xiang Zhang Lu-Sheng Xin Enrico Bortoletto K. Mathias Wegner Chong-Ming Wang |
| author_sort | Chang-Ming Bai |
| collection | DOAJ |
| description | The highly versatile group of Herpesviruses cause disease in a wide range of hosts. In invertebrates, only two herpesviruses are known: the malacoherpesviruses HaHV-1 and OsHV-1 infecting gastropods and bivalves, respectively. To understand viral transcript architecture and diversity we first reconstructed full-length viral genomes of HaHV-1 infecting <i>Haliotis diversicolor supertexta</i> and OsHV-1 infecting <i>Scapharca broughtonii</i> by DNA-seq. We then used RNA-seq over the time-course of experimental infections to establish viral transcriptional dynamics, followed by PacBio long-read sequencing of full-length transcripts to untangle viral transcript architectures at two selected time points. Despite similarities in genome structure, in the number of genes and in the diverse transcriptomic architectures, we measured a ten-fold higher transcript variability in HaHV-1, with more extended antisense gene transcription. Transcriptional dynamics also appeared different, both in timing and expression trends. Both viruses were heavily affected by post-transcriptional modifications performed by ADAR1 affecting sense-antisense gene pairs forming dsRNAs. However, OsHV-1 concentrated these modifications in a few genomic hotspots, whereas HaHV-1 diluted ADAR1 impact by elongated and polycistronic transcripts distributed over its whole genome. These transcriptional strategies might thus provide alternative potential roles for sense-antisense transcription in viral transcriptomes to evade the host’s immune response in different virus–host combinations. |
| first_indexed | 2024-03-10T06:08:19Z |
| format | Article |
| id | doaj.art-3b25b797b0ca41459ffa9c187e8eb16e |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-10T06:08:19Z |
| publishDate | 2021-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-3b25b797b0ca41459ffa9c187e8eb16e2023-11-22T20:18:49ZengMDPI AGViruses1999-49152021-09-011310197110.3390/v13101971Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional EditingChang-Ming Bai0Umberto Rosani1Xiang Zhang2Lu-Sheng Xin3Enrico Bortoletto4K. Mathias Wegner5Chong-Ming Wang6Key Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture, Qingdao Key Laboratory of Mariculture Epidemiology and Biosecurity, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266237, ChinaCoastal Ecology Section, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Warden Sea Station, 25992 List auf Sylt, GermanyKey Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture, Qingdao Key Laboratory of Mariculture Epidemiology and Biosecurity, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266237, ChinaKey Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture, Qingdao Key Laboratory of Mariculture Epidemiology and Biosecurity, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266237, ChinaDepartment of Biology, University of Padova, 35121 Padova, ItalyCoastal Ecology Section, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Warden Sea Station, 25992 List auf Sylt, GermanyKey Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture, Qingdao Key Laboratory of Mariculture Epidemiology and Biosecurity, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266237, ChinaThe highly versatile group of Herpesviruses cause disease in a wide range of hosts. In invertebrates, only two herpesviruses are known: the malacoherpesviruses HaHV-1 and OsHV-1 infecting gastropods and bivalves, respectively. To understand viral transcript architecture and diversity we first reconstructed full-length viral genomes of HaHV-1 infecting <i>Haliotis diversicolor supertexta</i> and OsHV-1 infecting <i>Scapharca broughtonii</i> by DNA-seq. We then used RNA-seq over the time-course of experimental infections to establish viral transcriptional dynamics, followed by PacBio long-read sequencing of full-length transcripts to untangle viral transcript architectures at two selected time points. Despite similarities in genome structure, in the number of genes and in the diverse transcriptomic architectures, we measured a ten-fold higher transcript variability in HaHV-1, with more extended antisense gene transcription. Transcriptional dynamics also appeared different, both in timing and expression trends. Both viruses were heavily affected by post-transcriptional modifications performed by ADAR1 affecting sense-antisense gene pairs forming dsRNAs. However, OsHV-1 concentrated these modifications in a few genomic hotspots, whereas HaHV-1 diluted ADAR1 impact by elongated and polycistronic transcripts distributed over its whole genome. These transcriptional strategies might thus provide alternative potential roles for sense-antisense transcription in viral transcriptomes to evade the host’s immune response in different virus–host combinations.https://www.mdpi.com/1999-4915/13/10/1971PacBio SMRTlong-read sequencingmalacoherpesvirusOsHV-1HaHV-1antisense transcription |
| spellingShingle | Chang-Ming Bai Umberto Rosani Xiang Zhang Lu-Sheng Xin Enrico Bortoletto K. Mathias Wegner Chong-Ming Wang Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing Viruses PacBio SMRT long-read sequencing malacoherpesvirus OsHV-1 HaHV-1 antisense transcription |
| title | Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing |
| title_full | Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing |
| title_fullStr | Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing |
| title_full_unstemmed | Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing |
| title_short | Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing |
| title_sort | viral decoys the only two herpesviruses infecting invertebrates evolved different transcriptional strategies to deflect post transcriptional editing |
| topic | PacBio SMRT long-read sequencing malacoherpesvirus OsHV-1 HaHV-1 antisense transcription |
| url | https://www.mdpi.com/1999-4915/13/10/1971 |
| work_keys_str_mv | AT changmingbai viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT umbertorosani viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT xiangzhang viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT lushengxin viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT enricobortoletto viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT kmathiaswegner viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting AT chongmingwang viraldecoystheonlytwoherpesvirusesinfectinginvertebratesevolveddifferenttranscriptionalstrategiestodeflectposttranscriptionalediting |