Parallel analysis of miRNAs and mRNAs suggests distinct regulatory networks in Crassostrea gigas infected by Ostreid herpesvirus 1

Abstract

Background Since 2008, the aquaculture production of Crassostrea gigas was heavily affected by mass mortalities associated to Ostreid herpesvirus 1 (OsHV-1) microvariants worldwide. Transcriptomic studies revealed the major antiviral pathways of the oyster immune response while other findings suggested that also small non-coding RNAs (sncRNA) such as microRNAs might act as key regulators of the oyster response against OsHV-1. To explore the explicit connection between small non-coding and protein-coding transcripts, we performed paired whole transcriptome analysis of sncRNA and messenger RNA (mRNA) in six oysters selected for different intensities of OsHV-1 infection. Results The mRNA profiles of the naturally infected oysters were mostly governed by the transcriptional activity of OsHV-1, with several differentially expressed genes mapping to the interferon, toll, apoptosis, and pro-PO pathways. In contrast, miRNA profiles suggested more complex regulatory mechanisms, with 15 differentially expressed miRNAs (DE-miRNA) pointing to a possible modulation of the host response during OsHV-1 infection. We predicted 68 interactions between DE-miRNAs and oyster 3′-UTRs, but only few of them involved antiviral genes. The sncRNA reads assigned to OsHV-1 rather resembled mRNA degradation products, suggesting the absence of genuine viral miRNAs. Conclusions We provided data describing the miRNAome during OsHV-1 infection in C. gigas. This information can be used to understand the role of miRNAs in healthy and diseased oysters, to identify new targets for functional studies and, eventually to disentangle cause and effect relationships during viral infections in marine mollusks.

Viral Decoys: The Only Two Herpesviruses Infecting Invertebrates Evolved Different Transcriptional Strategies to Deflect Post-Transcriptional Editing

“…This was the predominant situation in malacoherpesviruses, where 3 -UTRs appeared shorter compared to 5 -UTRs and generally not impacted by RTT. The propensity of miRNAs to target 3 -UTRs, and recent findings that miRNAs were differentially regulated during natural OsHV-1 infection of Crassostrea gigas [49], might suggest an adaptive benefit of shorter 3 -UTRs in escaping host defenses. For HaHV-1, 27% of the genome was predicted to contain AS gene overlaps, similar to what was reported for cytomegalovirus [20].…”

Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture

“…The Mir‐841 gene with 106 copies in O. edulis genome is involved in response to metabolic stress (Nischal et al, 2014 ) or virus (Moyo et al, 2017 ) in the plants. The involvement of several miRNAs in response to the herpes virus OsHV‐1 has been demonstrated in C. gigas (Rosani et al, 2020 ), Chlamys farreri (Chen et al, 2014 ). In O. edulis , miRNA involved in immune system regulation (miRNA1, miRNA10, miRNA8, miRNA33) has been shown to be regulated in response to B. ostreae (Martín‐Gómez et al, 2014 ).…”

Chromosomal assembly of the flat oyster (Ostrea edulisL.) genome as a new genetic ressource for aquaculture

“…The Mir-841 gene with 106 copies in O. edulis genome is known to be involved in the plants in response to metabolic stress (Nischal et al, 2014; Lu et al, 2014) or virus (Moyo et al, 2017). The involvement of several miRNAs in response to the herpes virus OsHV-1 have been demonstrated in C. gigas (Rosani et al, 2020), Chlamys farreri (Chen et al, 2014). In O. edulis , miRNA involved in immune system regulation (mi-RNA1, miRNA10, miRNA8, mi-RNA33, have been shown to be regulated in response to B. ostreae (Martin-Gomez et al, 2014).…”