Viral Transfer and Inactivation through Zooplankton Trophic Interactions

Abstract

Waterborne viruses are responsible for numerous diseases and are abundant in aquatic systems. Understanding the fate of viruses in natural systems has important implications for human health. This research quantifies the uptake of the bacteriophage T4 and the enteric virus echovirus 11 when exposed to the filter feeders Tetrahymena pyriformis and Daphnia magna, and also examines the potential of viral transfer due to trophic interactions. Experiments co-incubating each species with the viruses over 72–96 h showed up to a 4 log virus removal for T. pyriformis, while direct viral uptake by D. magna was not observed. However, viral uptake by D. magna occurred indirectly by viral transfer from prey to predator, through D. magna feeding on virus-loaded T. pyriformis. This prey–predator interaction resulted in a 1 log additional virus removal compared to removal by T. pyriformis alone. Incomplete viral inactivation by D. magna was observed through recovery of infective viruses from the daphnid tissue. This research furthers our understanding of the impacts of zooplankton filter feeding on viral inactivation and shows the potential for viral transfer through the food chain. The viral–zooplankton interactions observed in these studies indicate that zooplankton may improve water quality through viral uptake or may serve as vectors for infection by accumulating viruses.

Removal of Waterborne Viruses by Tetrahymena pyriformis Is Virus-Specific and Coincides with Changes in Protist Swimming Speed

“…All (RT-)­qPCR reactions were performed in duplicate, and each PCR run contained nontemplate controls (NTC) which were always negative. Previous work has shown the absence of PCR inhibition in our experimental protocol …”

“…Previous work has shown the absence of PCR inhibition in our experimental protocol. 30 For pooled virus experiments, (RT-)qPCR assays for each virus were checked against the other viruses included in a given experiment to ensure the specificity of the assay.…”

Waterborne Human Pathogenic Viruses in Complex Microbial Communities: Environmental Implication on Virus Infectivity, Persistence, and Disinfection

“…58,59 Filter-feeding zooplankton can uptake waterborne viruses like echovirus through prey− predator interactions, which may either facilitate virus removal and inactivation or act as a vector by transferring infectious viruses to higher trophic levels through the food chain. 53 Future research on the interactions of waterborne human pathogenic viruses and microbiome should broaden the scope from FLAs to other higher organisms, focusing on not only the risks of the microbes facilitating virus persistence and transport but also the benefits of higher organisms promoting virus removal and inactivation for water purification.…”

“…Besides FLAs, waterborne human pathogenic viruses can also interact with other higher organisms including nonamoeba protozoa, nematodes, and zooplankton in both natural and engineering water systems. Ciliates play a dual role in virus–ciliate interactions, activating or protecting internalized viruses, or facilitating virus removal and inactivation in water treatment, − possibly depending on both ciliate and virus species. Nematodes, which are well-known vectors of human pathogenic bacteria and protect ingested microorganisms from removal and inactivation in water treatment, were also reported transporting and protecting human coxsackievirus and echovirus. , Filter-feeding zooplankton can uptake waterborne viruses like echovirus through prey–predator interactions, which may either facilitate virus removal and inactivation or act as a vector by transferring infectious viruses to higher trophic levels through the food chain .…”

“…Ciliates play a dual role in virus–ciliate interactions, activating or protecting internalized viruses, or facilitating virus removal and inactivation in water treatment, − possibly depending on both ciliate and virus species. Nematodes, which are well-known vectors of human pathogenic bacteria and protect ingested microorganisms from removal and inactivation in water treatment, were also reported transporting and protecting human coxsackievirus and echovirus. , Filter-feeding zooplankton can uptake waterborne viruses like echovirus through prey–predator interactions, which may either facilitate virus removal and inactivation or act as a vector by transferring infectious viruses to higher trophic levels through the food chain . Future research on the interactions of waterborne human pathogenic viruses and microbiome should broaden the scope from FLAs to other higher organisms, focusing on not only the risks of the microbes facilitating virus persistence and transport but also the benefits of higher organisms promoting virus removal and inactivation for water purification.…”