Virivore

Last updated August 30, 2024

Virivore (equivalently virovore) comes from the English prefix viro- meaning virus, derived from the Latin word for poison^{[ citation needed ]}, and the suffix -vore from the Latin word vorare, meaning to eat, or to devour;^[1] therefore, a virivore is an organism that consumes viruses. Virivory is a well-described process in which organisms, primarily heterotrophic protists,^[2]^[3]^[4]^[5]^[6]^[7] but also some metazoans ^[8]^[9] consume viruses.

Discovery

Halteria sp. A species capable of virivory Halteria.jpg — *Halteria* sp. A species capable of virivory

The first described virovore was a small marine flagellate that was shown to ingest and digest virus particles.^[2] Subsequently, numerous studies directly and indirectly demonstrated the consumption of virions.^[3]^[4]^[5]^[6]^[7]^[8]^[9] In 2022, DeLong et al. showed that over the course of two days the ciliates Halteria and Paramecium reduced chlorovirus plaque-forming units by up to two orders of magnitude, supporting the idea that nutrients were transferred from the viruses to consumers.^[7]

Furthermore, the Halteria population grew with chlorovirus as the only source of nutrition, and grew minimally in the absence of chlorovirus.^[7] The Paramecium population, however, did not differ in growth when fed chloroviruses compared to the control group. Since the Paramecium population size remained constant in the presence of only cholorviruses, this indicated that Paramecium is capable of maintaining its population size, but not growing using chlorovirus as the sole carbon source. These data showed that some grazers can grow on viruses, but it does not apply to all grazers. It was estimated that Halteria consumed between 10,000 and 1,000,000 viruses per day. It's known that small protists, such as Halteria and Paramecium, are consumed by zooplankton indicating the movement of viral-derived energy and matter up through the aquatic food web. This contradicts the idea that the viral shunt limits the movement of energy up food webs by cutting off the grazer-microbe interaction. The amount of energy and matter passed up would depend on virion size and nutritional content, which would vary depending on the strain.

Biogeochemical impact

Viruses are the most abundant biological entities in the world's oceans.^[12]^[13]^[14] The life cycle of a lytic virus is an important process within the worlds oceans for the cycling of dissolved organic matter and particulate organic matter, i.e. the viral shunt.^[15]^[12]^[13] Viral particles themselves also make up a large proportion of the nitrogen and phosphorus rich particles within the dissolved organic matter pool, as they are made up of lipids, amino acids, nucleic acids, and likely carbon incorporated from host cells.^[12]^[13] It's considered that viruses can complement a grazers diet if ingested, and the microbe is not infected.^[14]

General grazing on viruses is widespread throughout the marine environment, with grazing rates as high as 90.3 mL⁻¹ day⁻¹.^[12] When both bacteria and viruses are present, viruses can be ingested at rates comparable to bacteria.^[2]

Using Oikopleura dioica and Equid alphaherpesvirus 1 (EhV) as a model, scientists estimated the nutritional gain from viruses;^[12]

24.2 ng C individual⁻¹ day⁻¹^[12]
2.8 ng N individual⁻¹ day⁻¹^[12]
0.2 ng P individual⁻¹ day⁻¹^[12]

It's suggested that in smaller grazers, viruses could potentially have a more significant impact on host nutrition.^[12] For example, in nanoflagellates, the estimated contribution is 9% carbon, 14% nitrogen, and 28% phosphorus.^[12]

While smaller bacteria are the ideal food source for grazers due to their size and carbon content, viruses are small, non-motile, and extremely abundant for grazers making them an alternative nutritional choice.^[14] For general grazers, to obtain the same amount of carbon from viruses that they get from bacteria, they would need to consume 1000 times more viruses.^[14] This does not make viruses the ideal carbon source for grazers. However, there are other benefits to consuming viruses besides growth. Studies show that digested viral particles release amino acids that the grazer can then utilize during their own polypeptide synthesis.^[14]

The viral sweep

Trophic interactions between grazers, bacteria, and viruses are important in regulating nutrient and organic matter cycling.^[14] The viral sweep is a mechanism in which grazers cycle carbon back into the classical food web by ingesting viral particles.^[12] Infection of host cells leads to the release of viral progeny, which are subsequently consumed by grazers.^[12] Grazers are then consumed by higher trophic organisms, therefore cycling carbon from viruses back into the classical food web and to higher trophic levels.^[12]

The viral sweep could be affected by many factors such as the size and abundance of the viral particles.^[12] The size of the virus will effect the elemental content of the virus particles.^[13] For example, a virus with a larger capsid will contribute more carbon, and viruses with larger genomes will contribute more nitrogen and phosphorus as a result of the increased nucleic acids.^[13] Additionally, the impact of the viral sweep could be more significant if grazers preying on bacteria infected with viruses are also considered.^[14] Overall, by consuming bacteria and viruses, grazers play an important role in cycling carbon.^[14]

Viral grazing

The consumption of viruses is largely based on the feeding behaviour of the organism.

Filter feeding

Filter feeding is a type of suspension feeding.^[16] Filter feeders usually actively capture single food particles on cili, hairs, mucus, or other structures.^[16] Researchers used Salpingeoca as a model filter feeder to observe change in viral abundance. Salpingeoca produce lorica to help them attach to the substrate.^[14] They also have one flagellum to create a water current which transports small particles towards them where tiny pseudopodia engulf the prey particles.^[14] When viruses were co-incubated with Salpingeoca, viral abundances decreased steadily over 90 days, showing that filter feeding is an effective mechanism for feeding on viruses.^[14]

Grazing on sediment particles

Grazers move over surfaces to gather and ingest food as they go.^[16] Researchers used Thaumatomonas coloniensis as a model grazer to observe changes in viral abundances.^[14]T. coloniensis glides along the substrate and produce filopodia, which are used to engulf particles associated with the substrate.^[14] Over the 90 days, viral abundances steadily decreased when co-incubated with T. coloniensis, showing that grazing is an effective mechanism for feeding on viruses.^[14]

Raptorial feeding

Raptorial feeding is a form of active feeding, in which the organism seeks out its prey.^[14] Researchers used Goniomonas truncata as a model of raptorial feeding.^[14]G. truncata is a cryptomonad that has two flagella which are used to swim close to the substrate searching for food, and they have vacuoles to aid in food uptake.^[14] In the presence of G. truncata, viral abundances did not significantly decrease over the course of 90 days.^[14] However, this does not exclude the possibility that viral particles are taken up, and then released back into the environment.^[14] This data shows that raptorial feeding may not be a method of viral grazing, but it may have other ecological implications in terms of viral transmission.

Selective grazing

Grazing on viruses differs between viruses, and therefore it is subject to selective feeding. Flagellates are capable of ingesting many viruses of different sizes, with the smallest viruses having the lowest ingestion rate.^[2] There is huge diversity amongst marine viruses, including size, shape, morphology, and surface charge that may influence the selection, and therefore ingestion rates.^[2] Additionally, digestion rates of different viruses by the same flagellate were variable. This implies selection when grazing on viruses.^[2] For example, significant differences in virus removal by Tetrahymena pyriformis was observed when the protist was co-incubated with 13 different types of viruses.^[17] Additionally, the removal rates for the specific viruses were maintained when the protist was co-incubated with multiple viruses at once.^[17]T. pyriformis were able to identify viruses as food, which drives their movement and consumption of certain viruses over others, supporting the idea that some protists are capable of selective grazing.^[17]

Impact of viral infection on grazing

Viruses have the capacity to influence the grazing of their host cells during infection, showing that viral infection plays a role in selective grazing.^[18]^[19]

Copepods are a key link in marine food webs as they connect primary and secondary production with higher trophic levels.^[18] When phytoplankton Emiliania huxleyi were infected with the coccolithovirus EhV-86, ingestion of the infected cells by the calanoid copepod Acartia tonsa was significantly reduced compared to non-infected cells, indicating selective grazing against infected cells.^[18] These results suggest that viral infections reduce grazing, and may potentially reduce food web efficiency by keeping the carbon within the viral shunt-microbial loop, and inhibiting the movement of carbon to higher trophic levels.^[18] This emphasizes the importance of the viral sweep for cycling carbon into higher trophic levels.

Conversely, Oxyrrhis marina had a grazing preference for virally infected Emiliania huxleyi.^[19] It's suggested that the preference of infected cells over non-infected cells is due to physiological changes or change in size of the host cell.^[19]O. marina prefer to graze on larger cells as they could potentially get a greater nutritional value from them compared to a smaller cell, which would require the same amount of energy to consume.^[19] Infected E. huxleyi exhibit increased cell size compared to non-infected, making them an ideal prey for O. marina.^[19] Infected E. huxleyi may also be selected for their palatability as a result of physiological changes during infection.^[19] For example, infected cells will have higher nucleic acid content compared to non-infected cells which could improve the nutritional gain to the grazers.^[19] Additionally, grazing activity of O. marina has been linked to prey with lower dimethylsulfoniopropionate lyase (DMSP lyase) activity, as they would produce less of the potentially toxic compound acrylate.^[19] Virally infected E. huxleyi show reduced levels of DMSP lyase activity, which makes them appealing to O. marina by reducing their exposure to harmful compounds.^[19] Lastly, chemical cues such as the release of dimethyl sulfide and hydrogen peroxide during infection likely generate a gradient, making it easier for O. marina to locate the infected E. huxleyi.^[19] Preferential grazing on infected cells would make the carbon available to higher trophic levels by sequestering it in particulate form.^[19]

Overall, grazing on virus particles and virally infected cells are subject to selective grazing.

Ecological significance

Studies have shown that viruses may be ingested and digested, or ingested and released back into the environment by grazers.^[14]^[20] The observation that grazers could potentially release viruses back into the environment after ingestion could have significant ecological impacts.^[20]

Mode of transmission

The ingestion and release of viruses could mediate the transmission and dispersal of viruses in the marine environment.^[20] Using copepods as the model transmission vector, and EhV as the model virus, Frada et al. identified a potential mechanism of viral dispersal in marine environments.^[20]

EhV particles can be consumed by copepods either as individual virion particles or via host cell infection (in this case, infected Emiliania huxleyi).^[20] When infected E. huxleyi was co-incubated with copepods, the fecal pellets produced by the copepods contained an average of 4500 EhVs per pellet.^[20] These virion containing pellets were then co-incubated with a fresh culture of E. huxleyi, and rapid viral-mediated lysis of the host cells was observed.^[20] When EhV particles alone were co-incubated with copepods, i.e. no E. huxleyi, the fecal particles collected did not contain any virion particles.^[20] However, when they fed copepods EhV and Thalassiosira weissflogii , a diatom outside the host range of EhV, the fecal pellets collected contained 200 EhVs per pellet.^[20] These pellets when co-incubated with a fresh E. huxleyi culture were highly infectious and completely killed the culture.^[20] The absence of virion particles in the fecal pellets produced from sole EhV incubation supports the idea that grazers exhibit selective grazing for viruses. EhV can still be taken up by copepods through host cell infection and when in the presence of an ideal food source.^[20] Since viral abundance follows bacterial abundance, it is unlikely that there will be a marine environment where viruses will be the sole nutrient source for grazers.^[21]

The results of this experiment have significant ecological impacts. Copepods are capable of moving up and down the water column, and migrating short distances between feeding zones.^[20]^[22] Specifically, for copepods and EhV, the movement of copepods can transport viruses into new and non-infected populations of E. huxleyi, promoting bloom demise.^[20] Additionally, fecal pellets can sink from the mixed layer into deeper parts of the ocean, where they can be assimilated multiple times.^[22] These two scenarios represent potential mechanisms in which viruses can be introduced into new marine environments.

Non-host organisms

Grazers are not the only organisms capable of removing viruses from the water column. Non-host organisms such as anemones, polychaeta larvae, sea squirts, crabs, cockles, oysters, and sponges are all capable of significantly reducing the viral abundance.^[23] Sponges were found to have the greatest potential for removing viruses.^[23]

The method in which non-host organisms disrupt the viral-host contact is known as transmission interference.^[23] Non-host organisms can either have a direct impact by removing the host-organisms, or an indirect one by removing the viruses.^[23] These mechanisms cause a reduction in the virus-host contact rates which could significantly impact local microbial population dynamics.^[23]

Non-host organisms are capable of removing viruses at rates comparable to natural food particles, bacterial cells, and algal cells, which is higher when compared to grazers that have a viral clearance rate around 4%.^[2]^[23] In regions of high sponge densities, such as coastal and tropical regions, it is likely that the virus removal rate has been underestimated.^[23] The effective removal of viruses likely has global ecological impacts that have gone unrecognized.^[23]

Related Research Articles

Plankton are the diverse collection of organisms that drift in water but are unable to actively propel themselves against currents. The individual organisms constituting plankton are called plankters. In the ocean, they provide a crucial source of food to many small and large aquatic organisms, such as bivalves, fish, and baleen whales.

Coccolithophores, or coccolithophorids, are single-celled organisms which are part of the phytoplankton, the autotrophic (self-feeding) component of the plankton community. They form a group of about 200 species, and belong either to the kingdom Protista, according to Robert Whittaker's five-kingdom system, or clade Hacrobia, according to a newer biological classification system. Within the Hacrobia, the coccolithophores are in the phylum or division Haptophyta, class Prymnesiophyceae. Coccolithophores are almost exclusively marine, are photosynthetic and mixotrophic, and exist in large numbers throughout the sunlight zone of the ocean.

Zooplankton are the animal component of the planktonic community, having to consume other organisms to thrive. Plankton are aquatic organisms that are unable to swim effectively against currents. Consequently, they drift or are carried along by currents in the ocean, or by currents in seas, lakes or rivers.

Copepods are a group of small crustaceans found in nearly every freshwater and saltwater habitat. Some species are planktonic, some are benthic, a number of species have parasitic phases, and some continental species may live in limnoterrestrial habitats and other wet terrestrial places, such as swamps, under leaf fall in wet forests, bogs, springs, ephemeral ponds, puddles, damp moss, or water-filled recesses of plants (phytotelmata) such as bromeliads and pitcher plants. Many live underground in marine and freshwater caves, sinkholes, or stream beds. Copepods are sometimes used as biodiversity indicators.

The biological pump (or ocean carbon biological pump or marine biological carbon pump) is the ocean's biologically driven sequestration of carbon from the atmosphere and land runoff to the ocean interior and seafloor sediments. In other words, it is a biologically mediated process which results in the sequestering of carbon in the deep ocean away from the atmosphere and the land. The biological pump is the biological component of the "marine carbon pump" which contains both a physical and biological component. It is the part of the broader oceanic carbon cycle responsible for the cycling of organic matter formed mainly by phytoplankton during photosynthesis (soft-tissue pump), as well as the cycling of calcium carbonate (CaCO₃) formed into shells by certain organisms such as plankton and mollusks (carbonate pump).

Coccoliths are individual plates or scales of calcium carbonate formed by coccolithophores and cover the cell surface arranged in the form of a spherical shell, called a coccosphere.

<i>Gephyrocapsa huxleyi</i> Unicellular algae responsible for the formation of chalk

Gephyrocapsa huxleyi, formerly called Emiliania huxleyi, is a species of coccolithophore found in almost all ocean ecosystems from the equator to sub-polar regions, and from nutrient rich upwelling zones to nutrient poor oligotrophic waters. It is one of thousands of different photosynthetic plankton that freely drift in the photic zone of the ocean, forming the basis of virtually all marine food webs. It is studied for the extensive blooms it forms in nutrient-depleted waters after the reformation of the summer thermocline. Like other coccolithophores, E. huxleyi is a single-celled phytoplankton covered with uniquely ornamented calcite disks called coccoliths. Individual coccoliths are abundant in marine sediments although complete coccospheres are more unusual. In the case of E. huxleyi, not only the shell, but also the soft part of the organism may be recorded in sediments. It produces a group of chemical compounds that are very resistant to decomposition. These chemical compounds, known as alkenones, can be found in marine sediments long after other soft parts of the organisms have decomposed. Alkenones are most commonly used by earth scientists as a means to estimate past sea surface temperatures.

Coccolithovirus is a genus of giant double-stranded DNA virus, in the family Phycodnaviridae. Algae, specifically Emiliania huxleyi, a species of coccolithophore,^{serve as natural hosts. There is only one described species in this genus: Emiliania huxleyi virus 86.}

Cafeteria roenbergensis is a small bacterivorous marine flagellate. It was discovered by Danish marine ecologist Tom Fenchel and named by him and taxonomist David J. Patterson in 1988. It is in one of three genera of bicosoecids, and the first discovered of two known Cafeteria species. Bicosoecids belong to a broad group, the stramenopiles, also known as heterokonts (Heterokonta) that includes photosynthetic groups such as diatoms, brown, and golden algae, and non-photosynthetic groups such as opalinids, actinophryid "heliozoans", and oomycetes. The species is found primarily in coastal waters where there are high concentrations of bacteria on which it grazes. Its voracious appetite plays a significant role in regulating bacteria populations.

Phycodnaviridae is a family of large (100–560 kb) double-stranded DNA viruses that infect marine or freshwater eukaryotic algae. Viruses within this family have a similar morphology, with an icosahedral capsid. As of 2014, there were 33 species in this family, divided among 6 genera. This family belongs to a super-group of large viruses known as nucleocytoplasmic large DNA viruses. Evidence was published in 2014 suggesting that specific strains of Phycodnaviridae might infect humans rather than just algal species, as was previously believed. Most genera under this family enter the host cell by cell receptor endocytosis and replicate in the nucleus. Phycodnaviridae play important ecological roles by regulating the growth and productivity of their algal hosts. Algal species such Heterosigma akashiwo and the genus Chrysochromulina can form dense blooms which can be damaging to fisheries, resulting in losses in the aquaculture industry. Heterosigma akashiwo virus (HaV) has been suggested for use as a microbial agent to prevent the recurrence of toxic red tides produced by this algal species. Phycodnaviridae cause death and lysis of freshwater and marine algal species, liberating organic carbon, nitrogen and phosphorus into the water, providing nutrients for the microbial loop.

The microbial loop describes a trophic pathway where, in aquatic systems, dissolved organic carbon (DOC) is returned to higher trophic levels via its incorporation into bacterial biomass, and then coupled with the classic food chain formed by phytoplankton-zooplankton-nekton. In soil systems, the microbial loop refers to soil carbon. The term microbial loop was coined by Farooq Azam, Tom Fenchel et al. in 1983 to include the role played by bacteria in the carbon and nutrient cycles of the marine environment.

The microbial food web refers to the combined trophic interactions among microbes in aquatic environments. These microbes include viruses, bacteria, algae, heterotrophic protists. In aquatic ecosystems, microbial food webs are essential because they form the basis for the cycling of nutrients and energy. These webs are vital to the stability and production of ecosystems in a variety of aquatic environments, including lakes, rivers, and oceans. By converting dissolved organic carbon (DOC) and other nutrients into biomass that larger organisms may eat, microbial food webs maintain higher trophic levels. Thus, these webs are crucial for energy flow and nutrient cycling in both freshwater and marine ecosystems.

Calanus finmarchicus is a species of copepod and a component of the zooplankton, which is found in enormous amounts in the northern Atlantic Ocean.

In the deep ocean, marine snow is a continuous shower of mostly organic detritus falling from the upper layers of the water column. It is a significant means of exporting energy from the light-rich photic zone to the aphotic zone below, which is referred to as the biological pump. Export production is the amount of organic matter produced in the ocean by primary production that is not recycled (remineralised) before it sinks into the aphotic zone. Because of the role of export production in the ocean's biological pump, it is typically measured in units of carbon. The term was coined by explorer William Beebe as observed from his bathysphere. As the origin of marine snow lies in activities within the productive photic zone, the prevalence of marine snow changes with seasonal fluctuations in photosynthetic activity and ocean currents. Marine snow can be an important food source for organisms living in the aphotic zone, particularly for organisms that live very deep in the water column.

Marine microorganisms are defined by their habitat as microorganisms living in a marine environment, that is, in the saltwater of a sea or ocean or the brackish water of a coastal estuary. A microorganism is any microscopic living organism or virus, which is invisibly small to the unaided human eye without magnification. Microorganisms are very diverse. They can be single-celled or multicellular and include bacteria, archaea, viruses, and most protozoa, as well as some fungi, algae, and animals, such as rotifers and copepods. Many macroscopic animals and plants have microscopic juvenile stages. Some microbiologists also classify viruses as microorganisms, but others consider these as non-living.

Oxyrrhis marina is a species of heterotrophic dinoflagellate with flagella that is widely distributed in the world's oceans.

The viral shunt is a mechanism that prevents marine microbial particulate organic matter (POM) from migrating up trophic levels by recycling them into dissolved organic matter (DOM), which can be readily taken up by microorganisms. The DOM recycled by the viral shunt pathway is comparable to the amount generated by the other main sources of marine DOM.

Marine viruses are defined by their habitat as viruses that are found in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Viruses are small infectious agents that can only replicate inside the living cells of a host organism, because they need the replication machinery of the host to do so. They can infect all types of life forms, from animals and plants to microorganisms, including bacteria and archaea.

Marine protists are defined by their habitat as protists that live in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Life originated as marine single-celled prokaryotes and later evolved into more complex eukaryotes. Eukaryotes are the more developed life forms known as plants, animals, fungi and protists. Protists are the eukaryotes that cannot be classified as plants, fungi or animals. They are mostly single-celled and microscopic. The term protist came into use historically as a term of convenience for eukaryotes that cannot be strictly classified as plants, animals or fungi. They are not a part of modern cladistics because they are paraphyletic.

Phytoplankton are characterized as organisms which are unable to swim against a current and produce their own organic carbon via photosynthesis. They are responsible for producing approximately 50 percent of the Earth’s primary productivity and are therefore crucial in maintaining both marine ecosystems and adding a significant amount of oxygen to the atmosphere. However, as with other organisms, phytoplankton are hosts to many diverse forms of parasites, including, but not limited to, fungal- and non-fungal zoosporic parasites, Dinoflagellates, Cercozoans, and viruses. Parasites use nutrients from their hosts, at that organisms expense, and display diverse methods of infection. Parasites can play integral roles in the dynamics and interactions between phytoplankton and their communities, such as controlling population abundance, distribution and biodiversity.

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