Removal of large viruses and their dispersal through fecal pellets of the appendicularian Oikopleura dioica during Emiliania huxleyi bloom conditions

Abstract

Despite their importance in shaping the structure and function of marine microbial food webs, little is known about factors regulating marine virus abundance. Previous work demonstrated clearance of laboratory-cultured Emiliania huxleyi virus by the appendicularian Oikopleura dioica; however, the applicability of this interaction to natural virus assemblages was not investigated. Here, we conducted controlled laboratory experiments using O. dioica and mesocosm water containing natural virus assemblages with high densities of virus, and measured removal of virus by O. dioica using both flow cytometry and molecular methods. Bayesian models based on flow cytometry quantification of virus particles demonstrated efficient removal of viruses (mean 90.3 mL ind−1 d−1), with a clearance efficiency of 42.6% relative to food algae. Molecular detection of virus removal by quantification of viral mcp gene copies revealed a mean clearance rate of 68.1 mL ind−1 d−1. Fecal pellets from these experiments demonstrated that viruses in fecal pellets retain infectivity despite passage through the O. dioica gut. Shotgun metavirome analysis demonstrated O. dioica removal of large virus groups, notably the Phycodnaviridae. The results demonstrate the removal of E. huxleyi virus from natural virus assemblages by O. dioica and the maintenance of viral infectivity when incorporated into fecal pellets, prompting further investigation on the fate of fecal-packaged viruses and their impact on host dynamics. Furthermore, our results indicate the generality of this interaction for other large algal viruses, raising questions about the implications of this mechanism of marine virus redistribution on the broader marine virus community.