14 research outputs found
The consumption of viruses returns energy to food chains
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 âpredatorâ 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 Halteriaâchlorovirus interaction can be viewed as a trophic interaction. Finally, we used fluorescent microscopy to confirm the ingestion of chloroviruses by ciliates
Size-dependent Catalysis of Chlorovirus Population Growth by a Messy Feeding Predator
Many chloroviruses replicate in endosymbiotic zoochlorellae that are protected from infection by their symbiotic host. To reach the high virus concentrations that often occur in natural systems, a mechanism is needed to release zoochlorellae from their hosts. We demonstrate that the ciliate predator Didinium nasutum foraging on zoochlorellae-bearing Paramecium bursaria can release live zoochlorellae from the ruptured prey cell that can then be infected by chloroviruses. The catalysis process is very effective, yielding roughly 95% of the theoretical infectious virus yield as determined by sonication of P. bursaria. Chlorovirus activation is more effective with smaller Didinia, as larger Didinia typically consume entire P. bursaria cells without rupturing them, precluding the release of zoochlorellae. We also show that the timing of Chlorovirus growth is tightly linked to the predator-prey cycle between Didinium and Paramecium, with the most rapid increase in chloroviruses temporally linked to the peak foraging rate of Didinium, supporting the idea that predator-prey cycles can drive cycles of Chlorovirus abundance
Catalysis of Chlorovirus Production by the Foraging of \u3ci\u3eBursaria truncatella\u3c/i\u3e on \u3ci\u3eParamecia bursaria\u3c/i\u3e Containing Endosymbiotic Algae
Chloroviruses are large viruses that replicate in chlorella-like green algae and normally exist as mutualistic endosymbionts (referred to as zoochlorellae) in protists such as Paramecium bursaria. Chlorovirus populations rise and fall in indigenous waters through time; however, the factors involved in these virus fluctuations are still under investigation. Chloroviruses attach to the surface of P. bursaria but cannot infect their zoochlorellae hosts because the viruses cannot reach the zoochlorellae as long as they are in the symbiotic phase. Predators of P. bursaria, such as copepods and didinia, can bring chloroviruses into contact with zoochlorellae by disrupting the paramecia, which results in an increase in virus titers in microcosm experiments. Here, we report that another predator of P. bursaria, Bursaria truncatella, can also increase chlorovirus titers. After two days of foraging on P. bursaria, B. truncatella increased infectious chlorovirus abundance about 20 times above the controls. Shorter term foraging (3 h) resulted in a small increase of chlorovirus titers over the controls and more foraging generated more chloroviruses. Considering that B. truncatella does not release viable zoochlorellae either during foraging or through fecal pellets, where zoochlorellae could be infected by chlorovirus, we suggest a third pathway of predator virus catalysis. By engulfing the entire protist and digesting it slowly, virus replication can occur within the predator and some of the virus is passed out through a waste vacuole. These results provide additional support for the hypothesis that predators of P. bursaria are important drivers of chlorovirus population sizes and dynamics
Chloroviruses lure hosts through long-distance chemical signaling
Chloroviruses exist in aquatic systems around the planet where they infect certain eukaryotic green algae that are mutualistic endosymbionts in a variety of protists and metazoans. Natural chlorovirus populations are seasonally dynamic but the precise temporal changes in these populations and the mechanisms that underlie them have, heretofore, been unclear. We recently reported the novel concept that predator/prey-mediated virus activation regulates chlorovirus population dynamics, and in the current manuscript demonstrate virus packaged chemotactic modulation of prey behavior.
Viruses have not previously been reported to act as chemotactic/chemo-attractive agents. Rather, viruses as extracellular entities are generally viewed as non-metabolically active spore-like agents that await further infection events upon collisions with appropriate host cells. That a virus might actively contribute to its fate via chemotaxis and change the behavior of an organism independent of infection is unprecedented
Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae
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 protist Paramecium bursaria by copepods resulted in a \u3e100-fold increase in the number of chloroviruses in 1 d. Copepod predation can be seen as an ecological âcatalystâ by increasing contacts between chloroviruses and their hosts, zoochlorellae (endosymbiotic algae that live within paramecia), thereby facilitating viral population growth. When feeding, copepods passed P. bursaria through their digestive tract only partially digested, releasing endosymbiotic algae that still supported viral reproduction and resulting in a virus population spike. A simple predatorâprey 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.
Movie file (.mp4) attached below
Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae
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 protist Paramecium bursaria by copepods resulted in a \u3e100-fold increase in the number of chloroviruses in 1 d. Copepod predation can be seen as an ecological âcatalystâ by increasing contacts between chloroviruses and their hosts, zoochlorellae (endosymbiotic algae that live within paramecia), thereby facilitating viral population growth. When feeding, copepods passed P. bursaria through their digestive tract only partially digested, releasing endosymbiotic algae that still supported viral reproduction and resulting in a virus population spike. A simple predatorâprey 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.
Movie file (.mp4) attached below
Predators Foraging on Endosymbiotic Containing Paramecium Catalyze Chloroviruses Population in the Ecosystem
For millions of years, viruses have played an important role due to their influence on marine ecosystems. With over 70% of Earthâs surface being covered by water, there is an enormous number of viruses that are yet to be discovered or thoroughly researched. Todayâs technology brings forth greater and more enhanced methods to study and prove the importance of the role of viruses as part of the marine community structure, both on a global and miniscule scale. Viruses influence the biogeochemical cycle, gene transfer, disruption of algal blooms, and evolution of aquatic organisms. Even difficult and harsh environmental conditions do not hinder the aquatic virusesâ role in the cycling of carbon and nutrients within the water. One motivation for focusing on specific viruses is that they can play a significant role in the environment, but especially if the virus might also infect humans. One group of viruses that meet both of these criteria is the chloroviruses (family Phycodnaviridae) that are unique and have been studied for about the last 40 years. They serve as an interesting model for large, icosahedral, double stranded DNA viruses (genomes between 270 to 370 kb), which infect eukaryotic algae and presumably influence the aquatic environment. Furthermore, certain chlorovirus members may possibly influence cognitive behaviors in humans; however, this aspect is still under study as there is much to learn about this possible aspect of the viruses. Chloroviruses are common in freshwater environments. They replicate in eukaryotic, single-celled, chlorella-like green algae, which exist naturally as endosymbionts of protists. The chloroviruses are not only extremely abundant but are also diverse. Increases in chlorovirus populations occur as more viruses come into contact with their hosts, and frequently, there are spikes in viral abundance. Ongoing experiments, including those described in this thesis, are trying to determine how contact between chloroviruses and their hosts occur in order to generate these chlorovirus fluctuations. In our research, we established that predators can feed on Paramecium bursaria, which naturally have virus particles attached to their outer cell membrane. P. bursaria harbor several hundred algae inside their cytoplasm, which are the host algae for many of the chloroviruses. In this thesis we show that predators of P. bursaria, like copepods, can release these algae by disrupting the paramecia by one of two methods. One method is referred to as âmessy feedingâ, which occurs when the copepods chew off part of the P. bursaria causing the zoochlorellae to be released into the water column where they can easily be infected by viruses. The second method is referred to as âwhole feedingâ in which the copepods consume the entire paramecium. This pathway is primarily responsible for increasing virus populations by increasing the contact between the virus and its host (zoochlorellae) inside the copepodâs gut. In addition, fecal pellets released by the copepods also have the ability to generate more virus and result in high viral populations. The second chapter of this thesis explains how copepods function as an âecological catalyst.â Additions groups of predators of P. bursaria were discovered which have both direct and indirect association with chlorovirus expansion and their host. In the third chapter, we establish that the ciliate Didinium nasutum is a predator that also forages on paramecia by messy feeding and that this also leads to an increase in chlorovirus populations. Furthermore, in this chapter, we examine the effect of the size of the didinium on viral population growth. Small size didinia have a highly positive effect on viral growth in the water system. The third group of predators of P. bursaria that we studied (chapter 4) are referred to as giant ciliates, including Bursaria truncatella. They prey on paramecia primarily by whole feeding, but occasionally exhibit messy feeding. Both of these methods help to slightly increase virus populations and sustain them in nature. Finally, in the last chapter, we compared several other possible predators to see if they had an effect on chlorovirus abundance. Only nematodes were shown to increase chlorovirus populations, but this is still under study
Predators Foraging on Endosymbiotic Containing Paramecium Catalyze Chloroviruses Population in the Ecosystem
For millions of years, viruses have played an important role due to their influence on marine ecosystems. With over 70% of Earthâs surface being covered by water, there is an enormous number of viruses that are yet to be discovered or thoroughly researched. Todayâs technology brings forth greater and more enhanced methods to study and prove the importance of the role of viruses as part of the marine community structure, both on a global and miniscule scale. Viruses influence the biogeochemical cycle, gene transfer, disruption of algal blooms, and evolution of aquatic organisms. Even difficult and harsh environmental conditions do not hinder the aquatic virusesâ role in the cycling of carbon and nutrients within the water. One motivation for focusing on specific viruses is that they can play a significant role in the environment, but especially if the virus might also infect humans. One group of viruses that meet both of these criteria is the chloroviruses (family Phycodnaviridae) that are unique and have been studied for about the last 40 years. They serve as an interesting model for large, icosahedral, double stranded DNA viruses (genomes between 270 to 370 kb), which infect eukaryotic algae and presumably influence the aquatic environment. Furthermore, certain chlorovirus members may possibly influence cognitive behaviors in humans; however, this aspect is still under study as there is much to learn about this possible aspect of the viruses. Chloroviruses are common in freshwater environments. They replicate in eukaryotic, single-celled, chlorella-like green algae, which exist naturally as endosymbionts of protists. The chloroviruses are not only extremely abundant but are also diverse. Increases in chlorovirus populations occur as more viruses come into contact with their hosts, and frequently, there are spikes in viral abundance. Ongoing experiments, including those described in this thesis, are trying to determine how contact between chloroviruses and their hosts occur in order to generate these chlorovirus fluctuations. In our research, we established that predators can feed on Paramecium bursaria, which naturally have virus particles attached to their outer cell membrane. P. bursaria harbor several hundred algae inside their cytoplasm, which are the host algae for many of the chloroviruses. In this thesis we show that predators of P. bursaria, like copepods, can release these algae by disrupting the paramecia by one of two methods. One method is referred to as âmessy feedingâ, which occurs when the copepods chew off part of the P. bursaria causing the zoochlorellae to be released into the water column where they can easily be infected by viruses. The second method is referred to as âwhole feedingâ in which the copepods consume the entire paramecium. This pathway is primarily responsible for increasing virus populations by increasing the contact between the virus and its host (zoochlorellae) inside the copepodâs gut. In addition, fecal pellets released by the copepods also have the ability to generate more virus and result in high viral populations. The second chapter of this thesis explains how copepods function as an âecological catalyst.â Additions groups of predators of P. bursaria were discovered which have both direct and indirect association with chlorovirus expansion and their host. In the third chapter, we establish that the ciliate Didinium nasutum is a predator that also forages on paramecia by messy feeding and that this also leads to an increase in chlorovirus populations. Furthermore, in this chapter, we examine the effect of the size of the didinium on viral population growth. Small size didinia have a highly positive effect on viral growth in the water system. The third group of predators of P. bursaria that we studied (chapter 4) are referred to as giant ciliates, including Bursaria truncatella. They prey on paramecia primarily by whole feeding, but occasionally exhibit messy feeding. Both of these methods help to slightly increase virus populations and sustain them in nature. Finally, in the last chapter, we compared several other possible predators to see if they had an effect on chlorovirus abundance. Only nematodes were shown to increase chlorovirus populations, but this is still under study
Size-dependent Catalysis of Chlorovirus Population Growth by a Messy Feeding Predator
Many chloroviruses replicate in endosymbiotic zoochlorellae that are protected from infection by their symbiotic host. To reach the high virus concentrations that often occur in natural systems, a mechanism is needed to release zoochlorellae from their hosts. We demonstrate that the ciliate predator Didinium nasutum foraging on zoochlorellae-bearing Paramecium bursaria can release live zoochlorellae from the ruptured prey cell that can then be infected by chloroviruses. The catalysis process is very effective, yielding roughly 95% of the theoretical infectious virus yield as determined by sonication of P. bursaria. Chlorovirus activation is more effective with smaller Didinia, as larger Didinia typically consume entire P. bursaria cells without rupturing them, precluding the release of zoochlorellae. We also show that the timing of Chlorovirus growth is tightly linked to the predator-prey cycle between Didinium and Paramecium, with the most rapid increase in chloroviruses temporally linked to the peak foraging rate of Didinium, supporting the idea that predator-prey cycles can drive cycles of Chlorovirus abundance
Chloroviruses lure hosts through long-distance chemical signaling
Chloroviruses exist in aquatic systems around the planet where they infect certain eukaryotic green algae that are mutualistic endosymbionts in a variety of protists and metazoans. Natural chlorovirus populations are seasonally dynamic but the precise temporal changes in these populations and the mechanisms that underlie them have, heretofore, been unclear. We recently reported the novel concept that predator/prey-mediated virus activation regulates chlorovirus population dynamics, and in the current manuscript demonstrate virus packaged chemotactic modulation of prey behavior.
Viruses have not previously been reported to act as chemotactic/chemo-attractive agents. Rather, viruses as extracellular entities are generally viewed as non-metabolically active spore-like agents that await further infection events upon collisions with appropriate host cells. That a virus might actively contribute to its fate via chemotaxis and change the behavior of an organism independent of infection is unprecedented