Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters

Abstract

Infectious diseases are mostly explored using reductionist approaches despite repeated evidence showing them to be strongly influenced by numerous interacting host and environmental factors. Many diseases with a complex aetiology therefore remain misunderstood. By developing a holistic approach to tackle the complexity of interactions, we decipher the complex intra-host interactions underlying Pacific oyster mortality syndrome affecting juveniles of Crassostrea gigas, the main oyster species exploited worldwide. Using experimental infections reproducing the natural route of infection and combining thorough molecular analyses of oyster families with contrasted susceptibilities, we demonstrate that the disease is caused by multiple infection with an initial and necessary step of infection of oyster haemocytes by the Ostreid herpesvirus OsHV-1 µVar. Viral replication leads to the host entering an immune-compromised state, evolving towards subsequent bacteraemia by opportunistic bacteria. We propose the application of our integrative approach to decipher other multifactorial diseases that affect non-model species worldwide.

Host‐microbiota interactions shed light on mortality events in the striped venus clam Chamelea gallina

“…Although multiple infections involving a virus cannot be excluded in C. gallina , the down‐regulation in both mortality sites of putative Interferon‐induced protein 44‐like (IFI44), a key element for effective antiviral defense in bivalve species (Olicard, Renault, Torhy, Benmansour, & Bourgougnon, ; Pauletto et al, ; Renault, Faury, Barbosa‐Solomieu, & Moreau, ; Segarra et al, ) and the significant down‐regulation of several pathways typically involved in virus response suggests that viral replications should be excluded in C. gallina . Furthermore, the absence of viral detection in the histological analysis carried out in our study supports the premise that viral replication is not at the root of C. gallina mortality as recently proposed in C. gigas (De Lorgeril et al, ).…”

“…While recent technological advances (e.g., next‐generation sequencing) have made it possible to obtain increasingly relevant information regarding the response to various environmental factors, even in nonmodel species, the interactions between hosts, their associated micro‐organisms and biotic and abiotic environmental factors have been minimally explored. These reductionist approaches have led to difficulties in deciphering multifactorial pathologies and mass mortality events affecting nonmodel species worldwide (de Lorgeril et al, ).…”

Dynamics of the Pacific oyster pathobiota during mortality episodes in Europe assessed by 16S rRNA gene profiling and a new target enrichment next‐generation sequencing strategy

“…Recently an elegant study carried out by de Lorgeril et al . () using experimental inoculations reproducing the natural route of infection in contrasting (susceptible vs. resistant) oyster families showed that the disease is caused by multiple infection with an initial and necessary step of infection of oyster haemocytes by the Ostreid herpesvirus OsHV‐1 μVar and subsequent bacteraemia by opportunistic bacteria. Accordingly, Lemire et al .…”

Potential of genomic selection for improvement of resistance to ostreid herpesvirus in Pacific oyster (Crassostrea gigas)

“…One of the main issues currently affecting oyster production worldwide is the ‘summer mortality syndrome’. This causes periodic mass mortality in farms worldwide and has been mainly attributed to a specific variant of the ostreid herpesvirus (OsHV‐1; Segarra et al ), amongst other factors (Malham et al ; Petton et al ; de Lorgeril et al ). Selective breeding to improve resistance to OsHV‐1 may have potential as a prevention strategy, and there is significant additive genetic variation in survival during OsHV‐1 infection, with estimated heritability values ranging from 0.12 to 0.63 (Dégremont et al ; Azéma et al ; Camara et al ; Gutierrez et al ).…”