Viral shunt

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The flow of DOM and POM through the food web, with the location of the viral shunt pathway noted Viral shunt.jpg
The flow of DOM and POM through the food web, with the location of the viral shunt pathway noted

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. [1]

Contents

Viruses can easily infect microorganisms in the microbial loop due to their relative abundance compared to microbes. [2] [3] Prokaryotic and eukaryotic mortality contribute to carbon nutrient recycling through cell lysis. There is evidence as well of nitrogen (specifically ammonium) regeneration. This nutrient recycling helps stimulate microbial growth. [4] As much as 25% of the primary production from phytoplankton in the global oceans may be recycled within the microbial loop through the viral shunt. [5]

Discovery and impact

Viral shunt was first described in 1999 by Steven W. Wilhelm and Curtis A. Suttle. [6] Their original paper has since been cited over 1000 times. [7] For his contributions to understanding of viral roles in marine ecosystems, Suttle has received numerous awards, including being named a Fellow of the Royal Society of Canada, receiving the A.G. Huntsman Award for Excellence in Marine Science, and the Timothy R. Parsons Medal for Excellence in Ocean Sciences from the Department of Fisheries and Oceans. [8] Both Suttle and Wilhelm [9] have been elected Fellows of the American Academy of Microbiology as well as the Association for the Sciences of Limnology and Oceanography (ASLO).

The field of marine virology has rapidly expanded since the mid-1990s, [10] coinciding with the first publication of viral shunt. During this time, further studies have established the existence of the viral shunt as a "fact" of the field. [10] The recycling of nutrients in the viral shunt has indicated to scientists that viruses are a necessary component in new models of global change. [11] Virologists in soil sciences have begun to investigate the application of viral shunt to explain nutrient recycling in terrestrial systems. [12] More recently, new theories concerning the potential role of viruses in carbon export - grouped under the idea of the "viral shuttle" have emerged. [13] While perhaps at odds on the surface, these theories are not mutually exclusive.[ citation needed ]

Bacterial growth efficiency

There is evidence to suggest that the viral shunt system can directly control bacterial growth efficiency (BGE) in pelagic regions. [14] Carbon flow models indicated that decreased BGE could be largely explained by the viral shunt, which caused the conversion of bacterial biomass to DOM. The biodiversity in these pelagic environments are so tightly coupled that the production of viruses depends on their bacterial host metabolisms, so any factors that limit bacterial growth also limit viral growth.[ citation needed ]

Enrichment of nitrogen has been observed to allow for an increase in viral production (up to 3-fold) but not bacterial biomass. [15] Through the viral shunt a high viral-induced mortality relative to bacterial growth resulted in the effective generation of DOC/DOM that is available for microbial re-consumption and offers an effective way to recycle key nutrients within the microbial food web.

Data extracted from other aquatic regions such as the Western-North Pacific displayed large variability, which may be a result of methodologies and environmental conditions. Nonetheless, a common trend appeared to be a reduced BGE with an increasing viral shunt pathway. [14] From carbon flow models it is clear that viral shunting allows bacterial biomass to be converted to DOC/DOM that are ultimately recycled such that the bacteria may consume the DOC/DOM, indicating that the viral shunt pathway is a major regulator of BGE in marine pelagic waters. [2] [16]

Microbial loop

The microbial loop acts as a pathway and connection between different relationships in an ecosystem. The microbial loop connects the pool of DOM to the rest of the food web, specifically various microorganisms in the water column. [17] This allows for constant cycling of this dissolved organic matter. Stratification of the water column due to the pycnocline affects the amount of dissolved carbon in the upper mixing layer, and the mechanisms shows seasonal variation.

The microbial loop is based on micro-interactions between different trophic levels of microbes and organisms. When nutrients enter the microbial loop, they tend to remain in the photic zone longer, due to the location, and slow sinking rates of microbes. Eventually, through varying processes, [18] DOM, through use of available nutrients, is produced by phytoplankton, as well as consumed by bacteria. [17] Bacteria utilize this DOM, yet are then preyed on by larger microbes, such as microflagellates, which helps to regenerate nutrients. [17]

Viruses tend to outnumber bacterial abundance by about ten times and phytoplankton by about a hundred times in the upper mixing layer [19] and bacterial abundance tends to decrease with depth, while phytoplankton remain closer to shallow depths. [20] The effects of the viral shunt are more pronounced in the upper mixing layer. Viruses found can be non-specific (broad host range), abundant, and can infect all forms of microbes. Viruses are a magnitude higher in abundance in almost all aquatic locations compared to their microbial hosts, allowing high rates/levels of microbial infection.

The impact of the viral shunt varies seasonally as many microbes show seasonal abundance maximums in temperate and oligotrophic waters during different times of the year, meaning viral abundance also varies with season. [21]

Biological pump

The viral shunt may result in increased respiration from the system. It also helps export carbon through the biological pump. This is a very significant process as approximately 3 gigatonnes of carbon may be sequestered per year due to lysed and virus-infected cells having faster sinking rates. [22] The biological pump has an important role at sequestering carbon to the benthic zone, thereby impacting global carbon cycles, budget, and even affecting temperature. Crucial nutrients, such as nitrogen, phosphorus, cellular components, such as amino acids and nucleic acids, would be sequestered through the biological pump in the event of cells sinking. [23] Viral shunting helps increase the efficiency of the biological pump by mostly altering the proportion of carbon that is exported to deep water (such as the recalcitrant carbon-rich cell walls from virally lysed bacteria) in a process called the Shunt and Pump. [23] This allows the crucial nutrients to be retained in the surface waters. Concurrently, a more efficient biological pump also results in an increase in nutrient influx towards the surface, which is beneficial to primary production, especially in more oligotrophic region. Despite viruses being in the smallest scales of biology, the viral shunt pathway has a profound effect on food webs across marine environments as well as on a more macro scale on the global carbon budget.

Recycling of nutrients

Carbon cycling

Viral shunt influences carbon cycling in marine environments by infecting microbes and redirecting the type of organic matter that enters the carbon pool. Phototrophs constitute a large population of primary production in marine environments and are responsible for a large flux of carbon entering the carbon cycle in marine environments. [24] However, bacteria, zooplankton and phytoplankton, (and other free-floating organisms) also contribute to the global marine carbon cycle. [25] When these organisms eventually die and decompose, their organic matter either enters the pool of particulate organic matter (POM) or dissolved organic matter (DOM). [23] Much of the POM generated is composed of carbon-rich complex structures that is unable to be decomposed effectively by most prokaryotes and archaea in the oceans. Export of carbon-rich POM from the upper surface layer to deep oceans causes increased efficiency of the biological pump due to a higher carbon-to-nutrient ratio. [23]

DOM is smaller and tends to stay mixed within the euphotic zone of the water column. The labile DOM is easier for microbes to digest and recycle, allowing incorporation of carbon into biomass.  As microbial biomass increases due to the incorporation of DOM, most microbial populations such as heterotrophic bacteria will be preyed on by organisms at higher trophic levels such as grazers or zooplankton. [5] However, about 20 to 40 percent of the bacterial biomass (with similar and relative amounts of eukaryotes) will become infected by viruses. [26] The effect of this energy flow results is less carbon entering higher trophic levels and a significant portion being respired and cycled between the microbes in the water column. [27]

Based on this mechanism, as more carbon enters the DOM pool, most of the matter is used for increasing microbial biomass. When the viral shunt kills a portion of these microbes, it decreases the amount of carbon that gets transferred to higher trophic levels by converting it back to DOM and POM. [27] Most of the generated POM is recalcitrant and will eventually make it down to the deep oceans where it accumulates. [23] The resulting DOM that re-enters the DOM pool to be used by phototrophs and heterotrophs is less than the amount of DOM that originally entered the DOM pool. This phenomenon is due to the unlikeliness of organic matter being 100% DOM after a viral lytic infection. [5]

Nitrogen cycling

Flow chart of nitrification in the deep ocean (aphotic zone) and ammonium regeneration in the upper ocean surface (photic zone) F ratio diagram.gif
Flow chart of nitrification in the deep ocean (aphotic zone) and ammonium regeneration in the upper ocean surface (photic zone)

Nitrogen cycle

Viral shunt is a big component to the cycling of nitrogen in marine environments. Nitrogen gas from the atmosphere gets dissolved into surface of the water. Nitrogen fixing cyanobacteria, such as Trichodesmium and Anabaena, convert the nitrogen gas (N2) into ammonium (NH4+) for microbes to use. The process of converting nitrogen gas to ammonia (and related nitrogen compounds) is called nitrogen fixation. The process of uptake of ammonium by microbes to be used in protein synthesis is called nitrogen assimilation. The viral shunt causes mass death of heterotrophic bacteria. The decomposition of these microbes releases particulate organic nitrogen (PON) and dissolved organic nitrogen (DON), which either stay in the upper mixing layer or sink to the deeper parts of the ocean. [28] In the deep ocean, PON and DON are converted back into ammonium by remineralisation. This ammonium can be used by deep ocean microbes, or undergo nitrification and be oxidized into nitrites and nitrates. [28] The sequence of nitrification is:

NH4+ → NO2− → NO3−

Dissolved nitrates can be consumed by microbes to become re-assimilated, or revert in nitrogen gas by denitrification. The resultant nitrogen gas can then be fixed back into ammonium for assimilation or exit the ocean reservoir and back into atmosphere. [28]

Ammonium regeneration

Viral shunt is also able to increase ammonium production. [29] The basis for this claim is based on fluctuating carbon-to-nitrogen (C:N in atoms) ratios caused by the viral shunt. Susceptible microorganisms such as bacteria in the water column are more likely to be infected and killed off by viruses, releasing DOM and nutrients containing carbon and nitrogen (about 4C:1N). The remaining microbes that are still alive are assumed to be resistant to that viral infection episode. The DOM and nutrients generated from the death and lysis of susceptible microorganisms are available for uptake by virus-resistant eukaryotes and prokaryotes. The resistant-bacteria uptakes and utilizes the DOC, regenerate ammonium, thereby lowering the C:N ratio. When C:N ratios decrease, ammonium (NH4+) regeneration increases. [30] The bacteria begin converting the dissolved nitrogen into ammonium, which can be used by phytoplankton for growth and biological production. As phytoplankton use up the ammonium (and subsequently limited by nitrogen-species), the C:N ratio begins increasing again and NH4+ regeneration slows down. [29] The phytoplankton also shows enhanced growth rates due to uptake of ammonium. [29] [31] The viral shunt is continuously causing changes to the C:N ratio, affecting the composition and presence of nutrients at any given time.

Iron cycling

A significant fraction of the world's oceans are iron limited, [32] thus the regeneration of iron-nutrients is an important process that is needed for sustaining an ecosystem in this environment. Viral infection of microorganisms (mostly heterotrophs and cyanobacteria) is hypothesized to be an important process in the maintenance of high-nutrient low chlorophyll (HNLC) marine environments. [33] The viral shunt plays a key role in releasing assimilated iron back into the microbial loop which helps sustain primary productivity in these ecosystems. [34] [35] Dissolved iron usually binds with organic matter to form an organic-iron complex that enhances bioavailability of this nutrient to plankton. [36] Some species of bacteria and diatoms are capable of high uptake rates of these organic-iron complexes. [33] Continued viral activity by the viral shunt helps sustain growing ecosystems in iron-limited HNLC regions. [33]

Effect on the marine food web

Viral shunt increases the supply of organic and inorganic nutrients to the pelagic food web. These nutrients increase growth rates of picophytoeukaryotes, particularly in multivore systems. Crucial nutrients such as nitrogen, phosphorus, and DOM found within cells are lysed by the viral shunt pathway, and these nutrients remain within the microbial food web. Naturally, this prevents the export of biomass such as POM to higher trophic levels directly, by diverting the flow of carbon and nutrients from all microbial cells into a DOM pool, recycled and ready for uptake. [37]

Viruses that specifically target cyanobacteria known as cyanophages (found in surface waters) directly affects the marine food web by "short-circuiting" the amount of organic carbon that is transferred to higher trophic levels. These nutrients are made available for uptake by heterotrophic bacteria and phytoplankton alike. [6]

The most common nutrient limiting primary productivity in marine waters is nitrogen, [38] and others such as iron, silica, and vitamin B12 have also been discovered to limit growth rate of specific species and taxa. [39] [40] [41] Studies have also identified that heterotrophic bacteria are commonly limited by organic carbon, [42] however some nutrients that limit growth may not limit in other environments and systems. Therefore, viral lysis of these nutrients will have different effects on microbial food webs found in different ecosystems. Another important point to note (on a smaller scale) is that cells contain different fractions of nutrients and cellular components; this will result in different bioavailability of certain nutrients in the microbial food web. [37]

A fluorescence microscopy image of a variety of picoplankton in the Pacific Ocean Picoplancton fluorescence Pacific.jpg
A fluorescence microscopy image of a variety of picoplankton in the Pacific Ocean

Important organisms

There are many different microbes present in aquatic communities. Phytoplankton, specifically Picoplankton, are the most important organism in this microbial loop. They provide a foundation as primary producers; they are responsible for the majority of primary production in the ocean and around 50% of primary production of the entire planet. [43]

Generally, marine microbes are useful in the microbial loop due to their physical characteristics. They are small, and have high surface area to biomass ratios, allowing for high rates of uptake, even in low concentrations of nutrients. The microbial loop is considered a sink for nutrients such as carbon. Their small size allows for more efficient cycling of nutrients and organic matter compared to larger organisms. [44] Additionally, microbes tend to be pelagic, floating freely in photic surface waters, before sinking down to deeper layers of the ocean. The microbial food web is important because it is the direct target of the viral shunt pathway and all subsequent effects are based on how the viruses affect their microbial hosts. Infection of these microbes through lysis or latent infection have a direct impact of the nutrients recycled, availability, and export within the microbial loop, which can have resonating effects throughout the trophic levels.

Shallow water hydrothermal vents

Shallow water hydrothermal vents found in the Mediterranean Sea contain a diverse and abundant microbial community known as "hotspots". [45] These communities also contain temperate viruses. An increase in these viruses can cause large mortality of vent microbes, thereby reducing chemoautotrophic carbon production, while at the same time enhancing the metabolism of heterotrophs through recycling of DOC. [46] These results indicate a tight coupling of viruses and primary/secondary production found in these hydrothermal vent communities, as well as having a major effect on the food web energy transfer efficiency to higher trophic levels.

See also

Related Research Articles

<span class="mw-page-title-main">Biological pump</span> Carbon capture process in oceans

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).

<span class="mw-page-title-main">Iron cycle</span>

The iron cycle (Fe) is the biogeochemical cycle of iron through the atmosphere, hydrosphere, biosphere and lithosphere. While Fe is highly abundant in the Earth's crust, it is less common in oxygenated surface waters. Iron is a key micronutrient in primary productivity, and a limiting nutrient in the Southern ocean, eastern equatorial Pacific, and the subarctic Pacific referred to as High-Nutrient, Low-Chlorophyll (HNLC) regions of the ocean.

<span class="mw-page-title-main">Dissolved organic carbon</span> Organic carbon classification

Dissolved organic carbon (DOC) is the fraction of organic carbon operationally defined as that which can pass through a filter with a pore size typically between 0.22 and 0.7 micrometers. The fraction remaining on the filter is called particulate organic carbon (POC).

<span class="mw-page-title-main">Picoplankton</span> Fraction of plankton between 0.2 and 2 μm

Picoplankton is the fraction of plankton composed by cells between 0.2 and 2 μm that can be either prokaryotic and eukaryotic phototrophs and heterotrophs:

<span class="mw-page-title-main">Microbial loop</span> Trophic pathway in marine microbial ecosystems

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.

<span class="mw-page-title-main">Sea surface microlayer</span> Boundary layer where all exchange occurs between the atmosphere and the ocean

The sea surface microlayer (SML) is the boundary interface between the atmosphere and ocean, covering about 70% of Earth's surface. With an operationally defined thickness between 1 and 1,000 μm (1.0 mm), the SML has physicochemical and biological properties that are measurably distinct from underlying waters. Recent studies now indicate that the SML covers the ocean to a significant extent, and evidence shows that it is an aggregate-enriched biofilm environment with distinct microbial communities. Because of its unique position at the air-sea interface, the SML is central to a range of global marine biogeochemical and climate-related processes.

<span class="mw-page-title-main">Marine snow</span> Shower of organic detritus in the 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.

<span class="mw-page-title-main">Bacterioplankton</span> Bacterial component of the plankton that drifts in the water column

Bacterioplankton refers to the bacterial component of the plankton that drifts in the water column. The name comes from the Ancient Greek word πλανκτος, meaning "wanderer" or "drifter", and bacterium, a Latin term coined in the 19th century by Christian Gottfried Ehrenberg. They are found in both seawater and freshwater.

<span class="mw-page-title-main">Marine microorganisms</span> Any life form too small for the naked human eye to see that lives in a marine environment

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.

<span class="mw-page-title-main">Mycoplankton</span> Fungal members of the plankton communities of aquatic ecosystems

Mycoplankton are saprotrophic members of the plankton communities of marine and freshwater ecosystems. They are composed of filamentous free-living fungi and yeasts that are associated with planktonic particles or phytoplankton. Similar to bacterioplankton, these aquatic fungi play a significant role in heterotrophicmineralization and nutrient cycling. Mycoplankton can be up to 20 mm in diameter and over 50 mm in length.

<span class="mw-page-title-main">Particulate organic matter</span>

Particulate organic matter (POM) is a fraction of total organic matter operationally defined as that which does not pass through a filter pore size that typically ranges in size from 0.053 millimeters (53 μm) to 2 millimeters.

<span class="mw-page-title-main">Marine biogeochemical cycles</span>

Marine biogeochemical cycles are biogeochemical cycles that occur within marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. These biogeochemical cycles are the pathways chemical substances and elements move through within the marine environment. In addition, substances and elements can be imported into or exported from the marine environment. These imports and exports can occur as exchanges with the atmosphere above, the ocean floor below, or as runoff from the land.

An oxygen minimum zone (OMZ) is characterized as an oxygen-deficient layer in the world's oceans. Typically found between 200 m to 1500 m deep below regions of high productivity, such as the western coasts of continents. OMZs can be seasonal following the spring-summer upwelling season. Upwelling of nutrient-rich water leads to high productivity and labile organic matter, that is respired by heterotrophs as it sinks down the water column. High respiration rates deplete the oxygen in the water column to concentrations of 2 mg/L or less forming the OMZ. OMZs are expanding, with increasing ocean deoxygenation. Under these oxygen-starved conditions, energy is diverted from higher trophic levels to microbial communities that have evolved to use other biogeochemical species instead of oxygen, these species include nitrate, nitrite, sulphate etc. Several Bacteria and Archea have adapted to live in these environments by using these alternate chemical species and thrive. The most abundant phyla in OMZs are Pseudomonadota, Bacteroidota, Actinomycetota, and Planctomycetota.

<span class="mw-page-title-main">Hydrothermal vent microbial communities</span> Undersea unicellular organisms

The hydrothermal vent microbial community includes all unicellular organisms that live and reproduce in a chemically distinct area around hydrothermal vents. These include organisms in the microbial mat, free floating cells, or bacteria in an endosymbiotic relationship with animals. Chemolithoautotrophic bacteria derive nutrients and energy from the geological activity at Hydrothermal vents to fix carbon into organic forms. Viruses are also a part of the hydrothermal vent microbial community and their influence on the microbial ecology in these ecosystems is a burgeoning field of research.

<span class="mw-page-title-main">Marine food web</span> Marine consumer-resource system

A marine food web is a food web of marine life. At the base of the ocean food web are single-celled algae and other plant-like organisms known as phytoplankton. The second trophic level is occupied by zooplankton which feed off the phytoplankton. Higher order consumers complete the web. There has been increasing recognition in recent years that marine microorganisms.

<span class="mw-page-title-main">Marine viruses</span> Viruses found in marine environments

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.

Curtis A. Suttle is a Canadian microbiologist and oceanographer who is a faculty member at the University of British Columbia. Suttle is a Distinguished University Professor who holds appointments in Earth & Ocean Sciences, Botany, Microbiology & Immunology and the Institute for the Oceans and Fisheries and a Fellow of the Royal Society of Canada. On 29 December, 2021 he was named to the Order of Canada. His research is focused on the ecology of viruses in marine systems as well as other natural environments.

Virivore comes from the English prefix viro- meaning virus, derived from the Latin word for poison, and the suffix -vore from the Latin word vorare, meaning to eat, or to devour; therefore, a virivore is an organism that consumes viruses. Virivory is a well-described process in which organisms, primarily heterotrophic protists, but also some metazoans consume viruses.

<span class="mw-page-title-main">Parasites of phytoplankton</span>

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.

References

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