Papers in the Biological Sciences
John P. DeLong http://orcid.org/0000-0003-0558-8213
James L. Van Etten http://orcid.org/0000-0002-5063-0049
Irina V. Agarkova https://orcid.org/0000-0003-3110-8471
David D. Dunigan https://orcid.org/0000-0001-9496-5396
Date of this Version
PNAS 2023 Vol. 120 No. 1 e2215000120
Viruses impact host cells and have indirect effects on ecosystem processes. Plankton such as ciliates can reduce the abundance of virions in water, but whether virus consumption translates into demographic consequences for the grazers is unknown. Here, we show that small protists not only can consume viruses they also can grow and divide given only viruses to eat. Moreover, the ciliate Halteria sp. foraging on chloroviruses displays dynamics and interaction parameters that are similar to other microbial trophic interactions. These results suggest that the effect of viruses on ecosystems extends beyond (and in contrast to) the viral shunt by redirecting energy up food chains.
Many known viruses cause diseases, and consequently, virology has long focused on viruses as pathogens. Viruses also affect ecosystem processes, however, by lysing microbes and causing the release of nutrients (i.e., the viral shunt) and through the indirect consequences of host mortality (1, 2). Both of these research domains place viruses as the top “predator” in their food chains, but like most predators, viruses also can serve as food. Many foragers that swallow water, soil particles, or leaves routinely ingest virus particles. Given the small mass of virus particles relative to other foods, the consumption of viruses is thought to be calorically unimportant (3, 4) and not of sufficient magnitude to influence ecosystem processes. Nonetheless, viruses contain amino acids, nucleic acids, and lipids (5), and if consumed in sufficient quantities could influence the population dynamics of the species that consume them. Some ciliates and flagellates may ingest many viruses (3, 4, 6, 7), but the demographic impact of virus consumption (virovory) is unclear. Here, we investigate the potential for virovory to fuel population growth and alter the pathways of energy flow in food webs. We measured the population growth of Halteria sp. and Paramecium bursaria in foraging trials with and without supplemental chloroviruses. We also tracked the reduction in chloroviruses and fit a classic trophic link model to the data to determine whether the Halteria–chlorovirus interaction can be viewed as a trophic interaction. Finally, we used fluorescent microscopy to confirm the ingestion of chloroviruses by ciliates.
Copyright © 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).