A novel birnavirus identified as the causative agent of summer atrophy of pearl oyster (Pinctada fucata (Gould))

PeerJ. 2024 Apr 30:12:e17321. doi: 10.7717/peerj.17321. eCollection 2024.

Abstract

The Akoya pearl oyster (Pinctada fucata (Gould)) is the most important species for pearl cultivation in Japan. Mass mortality of 0-year-old juvenile oysters and anomalies in adults, known as summer atrophy, have been observed in major pearl farming areas during the season when seawater temperatures exceed about 20 °C since 2019. In this study, we identified a novel birnavirus as the pathogen of summer atrophy and named it Pinctada birnavirus (PiBV). PiBV was first presumed to be the causative agent when it was detected specifically and frequently in the infected oysters in a comparative metatranscriptomics of experimentally infected and healthy pearl oysters. Subsequently, the symptoms of summer atrophy were reproduced by infection tests using purified PiBV. Infection of juvenile oysters with PiBV resulted in an increase in the PiBV genome followed by the atrophy of soft body and subsequent mortality. Immunostaining with a mouse antiserum against a recombinant PiBV protein showed that the virus antigen was localized mainly in the epithelial cells on the outer surface of the mantle. Although the phylogenetic analysis using maximum likelihood method placed PiBV at the root of the genus Entomobirnavirus, the identity of the bi-segmented, genomic RNA to that of known birnaviruses at the full-length amino acid level was low, suggesting that PiBV forms a new genus. The discovery of PiBV will be the basis for research to control this emerging disease.

Keywords: Birnavirus; Entomoviridae; Mass mortality; Pearl oyster; Pinctada birnavirus; Pinctada fucata.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Atrophy / virology
  • Birnaviridae* / genetics
  • Birnaviridae* / isolation & purification
  • Genome, Viral / genetics
  • Japan
  • Phylogeny
  • Pinctada* / genetics
  • Pinctada* / virology
  • Seasons

Grants and funding

This work was supported by the Food Safety and Consumer Affairs Bureau, the Ministry of Agriculture, Forestry, and Fisheries of Japan and JSPS KAKENHI Grant Numbers JP 22H02440. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.