Viruses are the most abundant “lifeforms” in the oceans, stretching up farther than the nearest 60 galaxies if placed end-to-end. Responsible for killing about 20 per cent of the oceanic microbial biomass daily, viruses have significant impacts on not only the marine ecosystems, but also the Earth’s climate. Here, we explore some of the complex interplays between marine viruses, their hosts, and the environment.
by Vanessa Lunardi
The world’s oceans are teeming with infection. A teaspoon of seawater typically contains about fifty million viruses1 and about every litre of seawater is home to about 100 billion viral particles2, adding up to about 1030 viruses worldwide. Every second, about 1023 viral infections take place in the ocean, which are a major source of disease and mortality in various organisms, ranging from shrimps to whales. But with every infection, new genetic information can also be introduced to an organism or progeny virus, hence driving the evolution of both host and virus.3
Evidently, apart from being arguably the most successful as they outnumber microbes—their typical hosts—10 to 1, they are also among the most important biological entities in the sea. However, scientists have yet to determine what most of them do, or even how many genetically distinct populations of viruses inhabit the seas.4 In this article, we probe into this vast reservoir of biological and genetic diversity, how they drive biogeochemical cycles, and interact with and regulate marine communities.
First seen as poisons, then as life-forms, and then as biological chemicals, viruses are small, infectious agents that can only replicate inside the living cells of a host organism.5 They can infect all types of life forms, from animals and plants to microorganisms, including bacteria and archaea.6 When not inside a cell or in the process of infecting a cell, these entities, which measure between 20 and 200 nanometres, exist in the form of independent particles called virions with incredibly simple structures.7
To date, there is divided opinion with regards to whether viruses are a form of life or merely organic structures with the capacity to interact with living organisms. Some regard them as “living” since they carry genetic material, reproduce by creating copies of themselves through self-assembly, and evolve through natural selection. However, because viruses lack some of the necessary cellular structures to count as "life", they have sometimes been described as replicators and “organisms at the edge of "life", existing in the grey area between living and non-living.
Besides the question of their being alive, the evolutionary history of viruses remains a fascinating, albeit murky, topic for cell biologists and virologists alike. Due to their immense diversity, the classification of these entities and their place in the conventional tree of life remain inconclusive. They may have begun as genetic elements that ultimately obtained the ability to move between cells, they may be previously free-living organisms that became parasites, or they may be the precursors of life as we know it.8
While very little is known about the origins of viruses, “The Virus-First Hypothesis” postulates that viruses may have been the first replicating entities that existed in a precellular world and predated or coevolved with their current cellular hosts.9 Several other viewpoints have emerged in scientific literature, but most concur that viruses have ancient origins. However, they were only discovered in the late 19th century and seen for the first time in the 1930s. Research in marine viruses only began thereafter, with the first phage being isolated from the North Sea in the 1950s10 and viruses being recognised as the causative agents of fish diseases, such as infectious pancreatic necrosis and Oregon sockeye disease in the 1960s.11 By the late 1970s, there had been persuasive evidence that viruses are prevalent in the sea.12 However, marine viruses remained largely overlooked by scientists until a decade later when viruses were revealed to be the most abundant biological entities in oceanic marine environments,2 thereby prompting scientists to consider their ecological impacts on the oceans.10 It was in the 1990s that scientists discovered that viruses can infect marine systems beyond plants and animals, such as bacteria and phytoplankton.13
With the increasing realisation of the importance and diversity of viruses in marine ecosystems, research in marine viruses further developed into a significant and independent field of study in marine biology. Through technical advances such as the development of molecular tools and DNA sequencing techniques, deep exploration of how viruses arose, their diversity, and the genetic mechanisms of virus-host interactions have become possible. In fact, virus research has now expanded into coral reefs, the deep biosphere, freshwater environments, and sediments with many investigations being done to determine their roles in driving algal and bacterial mortality, evolution at the nanoscale, and global-scale biogeochemical cycles and ocean productivity.13
Types of Marine Viruses and How They Interact with Their Hosts
Since the majority of marine viruses are bacteriophages, they are generally considered to be microbe killers. However, there are also significant numbers that infect eukaryotic phytoplankton, invertebrates, and vertebrates, the best studied of which are those that infect commercially important species.
With fish being particularly prone to infections, scientists have been intensely studying these viruses and have since discovered that at least nine types of rhabdovirus, which are distinct from but related to rabies virus, can infect economically important species including carp, cod, perch, pike, salmon, and sea bass, leading to anaemia, bleeding, lethargy, and even death.
In 1984, infectious salmon anaemia was discovered in Norway in an Atlantic salmon hatchery, where 80 per cent of the fish in the outbreak died, and has since been reported in Canada, Chile, the USA, the Faroe Islands, Ireland, the UK and Scotland. Although the viral outbreak in Scotland was successfully eradicated between 1998 and 1999, the virus remains a major threat to the viability of Atlantic salmon farming.14
Marine mammals are also susceptible to viral infections. Since the late 1970s, influenza infections have been reported in wild populations of cetaceans and pinnipeds as major causes of mass mortality.15 In 1988, the phocine distemper virus, which belongs to the Morbillivirus genus, caused an epidemic that resulted in 23,000 harbour seal deaths in northern Europe, and another one in 2002 leading to 30,000 deaths. In 2004, the virus was also confirmed in sea otters in the North Pacific Ocean.16,17 Belonging to the same genus, cetacean morbillivirus has been found to affect various species such as dolphins, porpoises, and whales in different parts of the world. Clinical signs of morbilliviruses in cetaceans include abnormal mentation, cachexia, and respiratory distress. The virus also causes erratic swimming, ocular and nasal discharge, pyrexia, and respiratory distress in pinnipeds.18
Many other viruses infect marine mammals among other organisms and even cause disease in humans, including adenoviruses, parvoviruses, and caliciviruses, albeit the natural reservoirs of most of these viruses are unknown.19 Besides, studies have revealed that marine viruses can infect coral, coral fish, and marine sponges by triggering the release and movement of nutrients, which may lead to altered reef ecosystem function and coral disease and mortality.
Interestingly, although viruses are most commonly known as mere killers that hijack the machinery inside the cell to replicate, not all phages immediately kill their hosts upon infection. In fact, studies involving chemical induction have revealed that about half of bacterial isolates from various marine environments contain prophages10 and bioinformatic analyses have shown that prophage-like elements exist in nearly 50 per cent of marine bacterial genomes.20
When a phage infects its host in a process known as lysogeny, the phage genome can be integrated into the bacterial chromosome or be maintained as “silent” plasmids within their host until an induction event triggers the prophage to become lytic. That is, some phages wait before lysing their hosts and instead, form a symbiotic relationship with their hosts.10 Phages can be protected from unfavourable conditions such as UV inactivation and proteolytic digestion by remaining in their hosts, while infected hosts, particularly that of bacteria, can develop resistance to superinfection by phages of the same kind or closely related phages. A study has also proposed that marine prophages may contribute to host survival in unfavourable environments by expressing phage-encoded auxiliary metabolic genes, which suppress unnecessary metabolic activities or regulate host gene expression.20
How Marine Viruses Drive Evolution, Shape Ecosystems, and Potentially Enhance Climate Change
The interactions between phage and host are evidently extremely diverse. Importantly, viruses are a crucial natural means of transferring genes between different species in the marine environment, which increases genetic diversity and drives evolution.
In the process of viral propagation, viruses transfer nucleic acid synthesised in one bacterium to another. If a virus infecting a new host contains genetic material from the previous host rather than its own DNA, the extra genetic information may be transmitted to the new host, resulting in transduction.
Although bacteriophage-mediated horizontal transduction has been known for nearly half a century and has been found to occur in many phage-host systems, previous studies have largely focused on the genetics of these viruses instead of their role in microbial ecology. In fact, gene transfer via transduction was considered negligible due to the lytic effect of phage infection. However, in the late 1980s,21 it was suggested that gene transduction may be as important or even more important than conjugation and transformation in the environment. Unlike DNA transformation, the process of DNA transduction usually involves genetic material being packaged inside protein shells called phage capsids. These capsids facilitate the safe delivery of the genome into the interior of the host cell as they protect the DNA from nuclease degradation. Through transduction and other means of DNA transfer, viruses serve as reservoirs for exogenous genes that can significantly alter the genetic diversity and composition of microbial populations.22
Viruses of marine bacteria also often contain auxiliary metabolic genes that modulate host cell metabolism during viral infection to help the phage replicate more efficiently. In fact, most cyanomyoviruses and some cyanopodoviruses have been shown to carry auxiliary metabolic genes that not only appear to maintain the photosynthetic machinery functional during infection, but also divert energy away from carbon fixation to nucleotide production for phage development.23 With marine picocyanobacteria of the genera Prochlorococcus and Synechococcus being the most numerous photosynthetic organisms on the planet, responsible for approximately 10 per cent of global primary production, altering the carbon-fixing capacity of these bacteria can significantly alter the global carbon cycle.
Besides inhibiting carbon fixation, viruses can alter elemental cycling, particularly that of carbon, through viral lysis. By rupturing algal and bacterial host cells, the materials contained within can be released and remain in the water column as dissolved organic or inorganic nutrients. Since carbon from cell lysis sinks more slowly, they can be retained to a greater extent in surface waters, where much of it will be converted to dissolved inorganic carbon by respiration or solar radiation. The living particulate organic carbon, however, can be used by other microorganisms to grow, after which it can be eaten by larger creatures like zooplankton and fish, which will, in turn, be eaten by sharks, whales and humans. In this manner, microscopic viruses play a vital role in recycling the materials necessary for life to flourish.7 In addition, virus-mediated cell lysis also liberates enough iron to supply the needs of phytoplankton, leading to the production of dimethyl sulphoxide, a gas that influences the climate of the Earth. Consequently, marine viruses have a significant impact on not only global microbial communities, but also geothermal cycles.24
By mediating the carbon cycle, marine viruses also influence the ocean’s ability to modulate the effects of climate change. Every year, about 12 gigatonnes of carbon, or a third of all man-induced carbon dioxide emissions, are put away by a special sequestration system known as the biological pump.25 The biological pump essentially removes carbon from the surface of the ocean water, converts it into living matter, and distributes it into the deeper water layers, where it is out of contact with the atmosphere. While viruses are now recognised to increase the efficiency of this process, this exact mechanism has only been recently revealed.
In the first global survey of marine RNA viruses, where thousands of new viruses were discovered, at least 11 were found to infect plankton that are important in absorbing carbon from the atmosphere and permanently storing it in the ocean floor.25 By attacking these organisms and injecting viral genetic material into them, viruses can change how these microbes process carbon.26 According to a 2016 study, marine cyanobacteria, which play a key role in “fixing” up to half of the carbon dioxide on Earth, are susceptible to infections by viruses that prevent carbon fixation. In fact, the researchers estimated that cyanobacteria-infecting viruses, or cyanophages, prevent the fixation of 20 million to 5.39 billion metric tons of carbon annually. The upper end of these numbers is equivalent to about 10 per cent of the carbon fixed every year by the entire ocean, or 5 per cent of the carbon fixed globally.26,27 By reducing carbon fixation, viruses can tip the scales toward more carbon dioxide and therefore, more global warming.
The effects of viruses on marine microbial communities and biogeochemical processes are countless. Despite the recent discoveries of novel viruses and new mechanisms underlying virus distribution and diversity, we have only started to venture into the fascinating world of marine viruses and how they interact with ecologically important environmental variables. With advancements in sequencing technologies and tools that can better measure the physical and chemical properties of the ocean, future investigations are expected to shed important insights into the role phages play in marine systems.
- Suttle, C. A. (2005, September 14). Viruses in the sea - Nature. Nature, www.nature.com. https://www.nature.com/articles/nature04160
- Bergh, Ø., BØrsheim, K., Bratbak, G. et al. High abundance of viruses found in aquatic environments. Nature, 340, 467–468 (1989). https://doi.org/10.1038/340467a0
- Suttle, C. Marine viruses — major players in the global ecosystem. Nature Reviews Microbiology, 5, 801–812 (2007). https://doi.org/10.1038/nrmicro1750
- Wu, K. J. (2019, April 25). Scientists just found 200,000 new marine viruses. Here’s why that matters | NOVA | PBS. PBS; www.pbs.org. https://www.pbs.org/wgbh/nova/article/200000-marine-viruses/
- Brussaard, C.P., Baudoux, AC., Rodríguez-Valera, F. (2016). Marine Viruses. In: Stal, L., Cretoiu, M. (eds) The Marine Microbiome. Springer, Cham. https://doi.org/10.1007/978-3-319-33000-6_5
- Koonin, E.V., Senkevich, T.G. & Dolja, V.V. The ancient Virus World and evolution of cells. Biology Direct, 1, 29 (2006). https://doi.org/10.1186/1745-6150-1-29
- Vaqué, D. (2021, January 26). Marine viruses: the tiny microbes that orchestrate life in the ocean. The Conversation; theconversation.com. https://theconversation.com/marine-viruses-the-tiny-microbes-that-orchestrate-life-in-the-ocean-153311
- Wessner, D. R. (2010) The Origins of Viruses. Nature Education, 3(9):37. https://www.nature.com/scitable/topicpage/the-origins-of-viruses-14398218/
- Koonin, E.V., Martin, W. (2005). On the origin of genomes and cells within inorganic compartments. Trends Genet, 21(12), 647-54. doi: 10.1016/j.tig.2005.09.006.
- Breitbart, M. (2012). Marine Viruses: Truth or Dare. Annual Review of Marine Sciences, 4, 425–48 (http://eebweb.arizona.edu/faculty/saleska/swes.410.510/readings/breitbart_2012_ truthordare_viruses_review.pdf)
- Crane, M., & Hyatt, A. (2011). Viruses of Fish: An Overview of Significant Pathogens. Viruses, 3(11), 2025–2046. https://doi.org/10.3390/v3112025
- Torrella F, Morita RY. (1979). Evidence by electron micrographs for a high incidence of bacteriophage particles in the waters of Yaquina Bay, oregon: ecological and taxonomical implications. Applied and Environmental Microbiology, 37(4), 774-8. doi: 10.1128/aem.37.4.774-778.1979.
- Middelboe, M., & Brussaard, C. (2017). Marine Viruses: Key Players in Marine Ecosystems. Viruses, 9(10), 302. https://doi.org/10.3390/v9100302
- Infectious Salmon Anaemia (ISA). (2007). The Fish Site. https://thefishsite.com/disease-guide/infectious-salmon-anaemia-isa
- Fereidouni, S., Munoz, O., Von Dobschuetz, S. et al. Influenza Virus Infection of Marine Mammals. EcoHealth 13, 161–170 (2016). https://doi.org/10.1007/s10393-014-0968-1
- VanWormer, E., Mazet, J.A.K., Hall, A. et al. Viral emergence in marine mammals in the North Pacific may be linked to Arctic sea ice reduction. Sci Rep 9, 15569 (2019). https://doi.org/10.1038/s41598-019-51699-4
- Goldstein, T., Mazet, J. A., Gill, V. A., Doroff, A. M., Burek, K. A., & Hammond, J. A. (2009). Phocine distemper virus in northern sea otters in the Pacific Ocean, Alaska, USA. Emerging infectious diseases, 15(6), 925–927. https://doi.org/10.3201/eid1506.090056
- Wellehan, J., & Cortes-Hinojosa, G. (2019). Marine Mammal Viruses. Fowler’s Zoo and Wild Animal Medicine Current Therapy, Volume 9, 597–602. https://doi.org/10.1016/B978-0-323-55228-8.00084-9
- Field, C. L. (2022). Parasitic Diseases of Marine Mammals - Exotic and Laboratory Animals - MSD Veterinary Manual. MSD Veterinary Manual; www.msdvetmanual.com. https://www.msdvetmanual.com/exotic-and-laboratory-animals/marine-mammals/parasitic-diseases-of-marine-mammals
- Paul, J. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas?. ISME J 2, 579–589 (2008). https://doi.org/10.1038/ismej.2008.35
- Zeph, L. R., Onaga, M. A., & Stotzky, G. (1988). Transduction of Escherichia coli by bacteriophage P1 in soil. Applied and Environmental Microbiology, 54(7), 1731–1737. https://doi.org/10.1128/aem.54.7.1731-1737.1988
- Jiang, S. C., & Paul, J. H. (1998). Gene transfer by transduction in the marine environment. Applied and environmental microbiology, 64(8), 2780–2787. https://doi.org/10.1128/AEM.64.8.2780-2787.1998
- Sieradzki, E., Ignacio-Espinoza, J.C., Needham, D. et al. (2019). Dynamic marine viral infections and major contribution to photosynthetic processes shown by spatiotemporal picoplankton metatranscriptomes. Nature Communications, 10, 1169. https://doi.org/10.1038/s41467-019-09106-z
- Racaniello, V. (2009, March 20). The abundant and diverse viruses of the seas. The Abundant and Diverse Viruses of the Seas; www.virology.ws. https://www.virology.ws/2009/03/20/the-abundant-and-diverse-viruses-of-the-seas/
- Dinneen, J. (2022, June 9). Ocean viruses: Huge survey finds thousands of previously undescribed microbes | New Scientist. Ocean Viruses: Huge Survey Finds Thousands of Previously Undescribed Microbes | New Scientist; www.newscientist.com. https://www.newscientist.com/article/2323643-thousands-of-previously-undescribed-viruses-found-by-huge-ocean-survey/
- McDonald, J. (2016, June 17). Ocean viruses may have impact on Earth’s climate | Science | AAAS. Ocean Viruses May Have Impact on Earth’s Climate | Science | AAAS; www.science.org. https://www.science.org/content/article/ocean-viruses-may-have-impact-earth-s-climate#:~:text= The%20ocean%20is%20full%20of,viruses%20can%20impact%20this%20process.
- Puxty, R. J., Millard, A. D., Evans, D. J., & Scanlan, D. J. (2016). Viruses Inhibit CO 2 Fixation in the Most Abundant Phototrophs on Earth. Current Biology, 26(12), 1585–1589. https://doi.org/10.1016/j.cub.2016.04.036