Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae

Abstract

Virus population growth depends on contacts between viruses and their hosts. It is often unclear how sufficient contacts are made between viruses and their specific hosts to generate spikes in viral abundance. Here, we show that copepods, acting as predators, can bring aquatic viruses and their algal hosts into contact. Specifically, predation of the protistParamecium bursariaby copepods resulted in a >100-fold increase in the number of chloroviruses in 1 d. Copepod predation can be seen as an ecological “catalyst” by increasing contacts between chloroviruses and their hosts, zoochlorellae (endosymbiotic algae that live within paramecia), thereby facilitating viral population growth. When feeding, copepods passedP. bursariathrough their digestive tract only partially digested, releasing endosymbiotic algae that still supported viral reproduction and resulting in a virus population spike. A simple predator–prey model parameterized for copepods consuming protists generates cycle periods for viruses consistent with those observed in natural ponds. Food webs are replete with similar symbiotic organisms, and we suspect the predator catalyst mechanism is capable of generating blooms for other endosymbiont-targeting viruses.

Chloroviruses

“…Therefore, the viruses are in good position to infect zoochlorellae if the paramecium cell, which can harbor 300-600 zoochlorellae [16], is ruptured either artificially or naturally by an aquatic predator. In fact, artificial disruption of paramecia, by either sonication or neutral detergents, leads to an increase in virus titers of~10 2 PFUs per zoochlorella 8 to 12 h later [228]. Interestingly, the chloroviruses do not attach to a symbiont-free species of Paramecium caudatum, which likely lacks the virus specific receptor [227].…”

“…Subsequence passage of the paramecia through the copepod digestive system results in the release of fecal pellets containing viable zoochlorellae and chloroviruses ( Figure 12). Incubation of these isolated fecal pellets leads to rapid virus amplification [228]. Longitudinal sections of the ciliary pits and virus particles are located in the tight space of a ciliary pit and between the cilia.…”

“…Currently, nothing is known about the nature of this attachment process. The accumulation of infectious virions on the cell surface, which can number in the hundreds [228], could occur through random contacts between P. bursaria and chlorovirus particles as the paramecia move through the water. However, ongoing experiments indicate that the chloroviruses release a chemotactic agent that attracts P. bursaria [197].…”

A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

“…Current research suggests giant viruses only comprise a small percentage of viruses (<1%) in most samples. However, virus densities can fluctuate based on contact with their host: for example, Chlorella viruses are much more abundant when their hosts, normally sequestered as endosymbionts of Paramecium bursaria , are made available as a consequence of predatory activity on the Paramecium [89]. Regardless, it is clear some families tend to be more common than others: in marine metagenomics samples Phycodnaviridae -related sequences were found to be highest in abundance, followed by Mimiviridae [90,91].…”

Size-dependent Catalysis of Chlorovirus Population Growth by A Messy Feeding Predator

“…Although many viruses (and other parasites) are considered in the context of their interactions with specific hosts, it is becoming clear that parasites in general are integral parts of food webs [3][4][5][6][7][8]. This is because food webs influence the abundance and distribution of hosts and because foraging interactions can influence the transmission, dispersal, and host encounter rates of parasites [5,9,10]. Thus, a variety of species interactions-including those not directly involved in a virus-host interaction-can influence virus activation and play a role in determining the structure of virus communities.…”