Temperature modulate disease susceptibility of the Pacific oyster Crassostrea gigas and virulence of the Ostreid herpesvirus type 1

Abstract

Temperature triggers marine diseases by changing host susceptibility and pathogen virulence. Oyster mortalities associated with the Ostreid herpesvirus type 1 (OsHV-1) have occurred seasonally in Europe when the seawater temperature range reaches 16-24 °C. Here we assess how temperature modulates oyster susceptibility to OsHV-1 and pathogen virulence. Oysters were injected with OsHV-1 suspension incubated at 21 °C, 26 °C and 29 °C and were placed in cohabitation with healthy oysters (recipients) at these three temperatures according to a fractional factorial design. Survival was followed for 14 d and recipients were sampled for OsHV-1 DNA quantification and viral gene expression. The oysters were all subsequently placed at 21 °C to evaluate the potential for virus reactivation, before being transferred to oyster farms to evaluate their long-term susceptibility to the disease. Survival of recipients at 29 °C (86%) was higher than at 21 °C (52%) and 26 °C (43%). High temperature (29 °C) decreased the susceptibility of oysters to OsHV-1 without altering virus infectivity and virulence. At 26 °C, the virulence of OsHV-1 was enhanced. Differences in survival persisted when the recipients were all placed at 21 °C, suggesting that OsHV-1 did not reactivate. Additional oyster mortality followed the field transfer, but the overall survival of oysters infected at 29 °C remained higher.

First comparison of French and Australian OsHV-1 µvars by bath exposure

“…Importantly, differences in outbreak temperature thresholds may be related to several factors, including methods to measure, analyze, and report water temperatures, other co-varying environmental factors, and oyster physiological condition and/or genetics (de Kantzow et al 2016). In our study, we maintained oysters at 22°C, a similar temperature profile to studies showing disease transmission and high levels of mortality in experimental studies in France (Schikorski et al 2011a,b, Delisle et al 2018 and Australia (Kirkland et al 2015, de Kantzow et al 2016, which may be an optimal temperature for full disease expression (de Kantzow et al 2016, Delisle et al 2018. However, to fully understand the oyster− virus relationship, a next step is to test oyster susceptibility to these viruses across a thermal gradient.…”

First evaluation of resistance to both a California OsHV-1 variant and a French OsHV-1 microvariant in Pacific oysters

“…While survival of the MBP families was high in this field trial, it reflects a single mortality event and the single count did not allow for a final mortality count; however, the plate assay results suggest that obtaining multiple mortality counts over time would not greatly alter this estimate of trait heritability. Furthermore, OsHV-1 survival is partly a function of temperature, so a longer elevated temperature event within permissive temperatures would likely cause greater mortality [1, 30, 31]. If strong genetic correlations do not exist between OsHV-1 survival influenced by temperature events of varying severity, field trials would be an ineffective resistance screening method as oyster growers desire OsHV-1 survival to the worst-case scenario.…”

Models with environmental drivers offer a plausible mechanism for the rapid spread of infectious disease outbreaks in marine organisms

“…Finally, we analyzed a third model in which transition from asymptomatic to full-fledged infection was triggered by accumulated stress following repeated or prolonged exposure to high temperatures. The two latter models were inspired by the environmentally-triggered transmission and pathology experienced by intertidal black abalone (Haliotis cracherodii) 44,45 and documented in other marine disease systems, such as the oyster Crassostrea gigas and Ostreid herpesvirus type 1 46,47 . The aim of our work was not to simulate the SSWD outbreak in detail, but to outline what transmission mechanism is most likely to reproduce spatiotemporal patterns similar to those observed in the 2013-15 outbreak.…”