Abstract

Massive mortality outbreaks affecting Pacific oysters (Crassostrea gigas) spat/juveniles are often associated with the detection of a herpesvirus called ostreid herpesvirus type 1 (OsHV-1). In this work, experimental infection trials of C. gigas spat with OsHV-1 were conducted using two contrasted Pacific oyster families for their susceptibility to viral infection. Live oysters were sampled at 12, 26, and 144 h post infection (hpi) to analyze host-pathogen interactions using comparative proteomics. Shotgun proteomics allowed the detection of seven viral proteins in infected oysters, some of them with potential immunomodulatoy functions. Viral proteins were mainly detected in susceptible oysters sampled at 26 hpi, which correlates with the mortality and viral load observed in this oyster family. Concerning the Pacific oyster proteome, more than 3,000 proteins were identified and contrasted proteomic responses were observed between infected A- and P-oysters, sampled at different post-injection times. Gene ontology (GO) and KEGG pathway enrichment analysis performed on significantly modulated proteins uncover the main immune processes (such as RNA interference, interferon-like pathway, antioxidant defense) which contribute to the defense and resistance of Pacific oysters to viral infection. In the more susceptible Pacific oysters, results suggest that OsHV-1 manipulate the molecular machinery of host immune response, in particular the autophagy system. This immunomodulation may lead to weakening and consecutively triggering death of Pacific oysters. The identification of several highly modulated and defense-related Pacific oyster proteins from the most resistant oysters supports the crucial role played by the innate immune system against OsHV-1 and the viral infection. Our results confirm the implication of proteins involved in an interferon-like pathway for efficient antiviral defenses and suggest that proteins involved in RNA interference process prevent viral replication in C. gigas. Overall, this study shows the interest of multi-omic approaches applied on groups of animals with differing sensitivities and provides novel insight into the interaction between Pacific oyster and OsHV-1 with key proteins involved in viral infection resistance.

Highlights

  • Ostreid herpesvirus type 1 (OsHV-1) represents a major threat to the economy of the oyster aquaculture industry, as it is the causal agent of a severe disease that leads to massive oyster mortality and significant economic losses [1,2,3]

  • MS/MS spectra were searched by SEQUEST through Proteome Discoverer 2.4 (Thermo Fisher Scientific Inc.) against a database consisting of Crassostrea gigas entries from NCBI (41447 entries in March 2020) and 116 entries from the Pacific oyster herpesvirus (Uniprot 2020-01)

  • Many interferon-induced protein 44-like (IFI44)-like isoforms, specific of the interferon-like pathway, were modulated in the more resistant Pacific oysters infected with OsHV-1 at 12 and 144 hpi

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Summary

Introduction

Ostreid herpesvirus type 1 (OsHV-1) represents a major threat to the economy of the oyster aquaculture industry, as it is the causal agent of a severe disease that leads to massive oyster mortality and significant economic losses [1,2,3]. Oyster families selected for their higher resistance or higher susceptibility to OsHV-1 have been developed and used broadly for other topics such as polyploids [16], breeding for OsHV-1 from different geographical origins [17], breeding for dual resistance [18, 19], or immunology [20]. In this context, we investigated in this study the viral infection using two contrasted families (high versus low resistance) to explore the genetic basis of a better resistance to the viral infection and to better understand the molecular response of the host to the viral infection

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