Since the late 1990s, scientists have woken up to the fact that it’s microbes who drive the marine food web, as well as the microbial loop and the viral shunt, and they may even be the dominating force in ocean biomes around the world. The microorganisms responsible include an awesome lineup of phytoplankton, bacteria, archaea, viruses and other marine microbes, all of whom – incidentally – face a constant struggle to eat, without themselves being eaten.
The wake-up is due largely to developments in environmental genomics – notably in the use of DNA-based techniques, and DNA barcodes – which have allowed researchers a glimpse into the freakish scale of microbe biomass and production. 1
What Are Marine Microbes?
Ocean microbes are tiny organisms typically measuring around 100 times smaller than the width of a hair, although some are bigger. On average there are at least one million microbial cells in every drop of seawater. 2 To put it more simply: in one teaspoon of seawater (5mL), you’ll find an average of 50 million viruses, 5 million bacteria and 5,000-15,000 small algae or phytoplankton. Or consider this: if all the marine viruses were stretched end to end, they would span a distance of 10 million light years.
What Do Microbes Do in the Ocean?
Marine microbes constitute around 70 percent of the ocean’s biomass. They are critical to nutrient recycling as they act as decomposers and remineralizers, breaking down dead cells into base nutrients and making them available to other life forms. Microorganisms (like cyanobacteria) account for almost all the photosynthesis that takes place in the ocean, and about 70 percent of all the oxygen produced on Earth. They also regulate the recycling of nitrogen and phosphorus, as well as carbon. 3 Without them, we would all be dead.
Microbes (the word is interchangeable with microorganisms) are incredibly diverse. There are hundreds of thousands – perhaps hundreds of millions – of different species, but that’s not all. Even within species, there are enormous differences in size, food habits, and other behavior. This combination of huge, incomprehensible numbers and baffling biodiversity makes microbes very difficult to properly distinguish, identify and track. Which is why the use of metagenomics has proved so useful to microbiologists in this field.
Microorganisms in the Marine Food Web
|Mesoplankton||0.2→20 mm||Copepods; Pteropods; Tunicata|
|Microplankton||20→200 µm||most Phytoplankton; Coccolithophores, Ciliates; large Protists|
|Nanoplankton||2→20 µm||Diatoms; Nanoflagellates; Dinoflagellates|
Source: Methods in Marine Zooplankton Ecology (1992). 4
Marine Microbes in the Classical Food Web
Let’s take a look at what marine microorganisms do in the classical food web.
Phytoplankton and Bacteria
Phytoplankton (algae) are the primary producers. They use a process called photosynthesis to produce food energy from sunlight.
The most prolific primary producers in the ocean are diatoms and cyanobacteria. It is estimated that, between them, diatoms (45 percent) together with the Prochlorococcus and Synechoccus species of cyanobacteria (50 percent) account for nearly all the ocean’s primary productivity (marine carbon fixation). Coccolithophores and autotrophic dinoflagellates are also important contributors to primary production. 5 6
During photosynthesis, chlorophyll – the green pigment in algae – captures energy from the sun. Because this requires sunlight, photosynthesis can only take place in the surface layer of the ocean. In the open ocean, this sunlit ‘euphotic’ layer is only about 100 meters in depth, above a water column that can be more than 3,000 meters deep.
Some of the solar energy captured is used to split water (H2O) into oxygen and hydrogen. The oxygen isn’t needed so this leaves the cell and ends up in the atmosphere. The hydrogen reacts with carbon dioxide (CO2) and, using more of the sun’s energy, forms glucose, which is stored in the algae’s body. (Also stored are nutrients absorbed from the water, such as nitrogen and phosphorus.)
The glucose food energy is then recycled in one of two ways. Either, the algae is eaten by zooplankton (who can’t make their own food) allowing the energy to pass up the food chain; or, the algae dies (they only live for a few days), in which case its remains drift in the upper layer before gradually sinking to the ocean floor (which can take weeks).
Usually, however, the remains are set upon by bacteria who break down the dead organic material into its component chemical nutrients, and then release the nutrients into the water for other organisms to eat. They use the CO2 for photosynthesis or other purposes, or else it escapes into the atmosphere. This decomposition process is known as remineralisation and it takes place mainly in surface waters. Bacteria are the only marine microbes capable of recycling this dead matter, which makes them a vital component in the health of the ecosystem.
If the dead algae sink below the surface layer and are remineralised in the deep ocean, the nutrients and CO2 remain in the deep ocean. This reduces the amount of CO2 in surface waters, allowing more CO2 to enter from the air, and thus helps to mitigate climate change by lowering CO2 levels in the atmosphere. The CO2 only returns to the atmosphere when ocean thermohaline circulation brings the deep water back to the surface, a journey which takes about 1,000 years.
This explains in brief the role of phytoplankton and the traditional role of bacteria although – as we shall see – there’s more to bacteria than meets the eye. The big deal about microscopic organisms like bacteria, is that they play a much more important role in the base of the ocean food chain that previously supposed. Originally, we paid only superficial attention to them. For example, we understood they helped to decompose waste and dead organic matter, but we thought they hung around in the water waiting for this material to appear. We now know this isn’t true: microbes are much more widespread and much more pro-active.
Carbon and Nutrient Cycling
In addition to the remains of phytoplankton algae, the upper layer of the ocean is full of other organic detritus, including: the remains of other organisms (zooplankton, fish, sea plants) fecal matter from living creatures, mucus secretions from zooplankton, mostly appendicularians, pteropods and salps) as well as other inorganic dust and nutrients. As these fragments (and the remains of the algae) sink into the ocean, they form what is known as “marine snow” because it looks like white fluffy snowflakes.
Most of this organic detritus is consumed by bacteria, zooplankton and other filter-feeding creatures, within the first 1,000 meters of its descent, but a small proportion of flakes – some of which can grow to several centimeters in diameter as they clump together with other flakes – reaches deeper water.
This continuous precipitation of organic matter provides food for numerous deep-sea creatures, and represents a significant energy export highway from the sunlit euphotic zone to the darker waters below, which is commonly described as the ‘biological pump’. Many animals in the dark depths of the sea, filter the food from the water or scavenge it on the seabed. Barnacles and mussels are seabed filter-feeders, while mobile scavengers include crabs, starfish, sea urchins and archaea.
The small percentage of material that is not consumed on the descent, or scavenged on the sea bottom, is incorporated into the muddy sediment covering the ocean floor. This sediment accumulates by about six meters (20 ft) every million years. 7
Dissolved Organic Carbon
As well as marine snow – the visible fragments of organic material – there’s a huge amount of microscopic carbon in the water. This is known as dissolved organic carbon (DOC). DOC is defined as micro-particles of organic carbon which can pass through a filter measuring between 0.22 and 0.7 micrometers. The larger-sized residue that remains on the filter is called particulate organic carbon (POC) which, being bigger, is more accessible to larger organisms. DOC is similar to dissolved organic matter (DOM) and particulate organic matter (POM) except it refers only to carbon matter. 8
DOC is a sort of food supplement or organic soup containing carbohydrates, fats, amino acids, sugars, proteins, enzymes or nucleic acids, that used to be part of living organisms. Typically, it has a high proportion of biodegradable dissolved organic carbon (BDOC), and is an ideal food source for the bacteria that decompose it and for other marine microbes who do not feed in the ordinary way, such as mollusc larvae.
Both marine snow and DOC represent important pathways in the carbon cycle, between the chemically active ocean surface and the relatively inert depths. As we saw, any carbon that reaches the deep ocean remains there until such time (perhaps 1,000 years later) as cold deep-water thermohaline currents upwell it to the surface.
However, much of the available organic carbon in both these cycles is taken up in the near-surface layer of the ocean, and acts as a major driver of the microbial loop.
The Microbial Loop
In the classical food web – or ‘grazer chain’ – phytoplankton are eaten by zooplankton, who in turn are eaten by fish, and so on.
In the microbial loop, the main food is not the algae but the microscopic particles of dissolved organic carbon (DOC) in the water. The dissolved organic carbon is assimilated by bacteria – such as the autotrophic bacteria Prochlorococcus or the heterotrophic bacteria Pelagibacter – who remineralize its other nutrients and release them into the water.
The bacteria is then eaten by other marine microbes like Nanoflagellates (zooplankton) who are eaten by other slightly larger zooplankton such as Ciliates. In due course, both the flagellates and the ciliates release DOC into the ocean, due to excretion or cell collapse, and so on. The microscopic size of the DOC particles prevents larger microorganisms from using them as a food source, so the DOC is really reserved exclusively for only the tiniest plankton, as well as bacteria and viruses.
It’s interesting to note that bacteria in the microbial loop operate in a similar way to phytoplankton in the classical food web, except instead of growing through photosynthesis of solar energy, they get their energy from DOC. The bacteria grow fat on DOC, thus turning themselves into a nice carbon sandwich for microzooplankton. And if these microzooplankton are then eaten by normal-sized zooplankton, the microbial loop will reconnect with the classical food web.
Who Are the Main Microorganisms in the Microbial Loop?
The two biggest actors in the microbial loop are bacteria and viruses.
There are 100 million times more bacteria in the ocean than stars in the known universe, and there are a thousand times more viruses than bacteria. 9
The ocean is filled with countless millions of bacteria (average size 1 millionth of a meter) who play a critical part in the marine food web. Some bacteria (the photoautotrophs) use sunlight for energy. Some (heterotrophs) prey on other organisms. Some (mixotrophs) use sunlight and prey on others for energy.
“Bacteria dominate the ocean in abundance, diversity and metabolic activity. The uptake of organic matter by bacteria is a major carbon-flow pathway, and its variability can change the overall flux of carbon in the ocean and, therefore, globally.” 10
Previously, scientists used to think that ocean bacteria were passive recipients of dissolved organic carbon (DOC), leaking from the grazing food chain, which they then fastened on, and mineralized. However, recent studies suggest that bacteria are far from passive and do not rely on DOC; they actually attack all carbon-based matter, even live microorganisms, in order to obtain energy. 11 In turn, they are preyed upon by viruses, flagellates and ciliates.
What is the Role of Bacteria in the Ocean?
Bacteria play several important roles in the microbial loop and the marine food web.
First, they take up more than half of all the organic carbon that comes from waste material in the classical food chain. This gives them critical value in the global carbon balance because they’re the only marine organisms capable of transforming and remineralizing this kind of waste. Many bacteria are saprotrophic, meaning they obtain energy from the organic material they consume, making the whole process super-efficient. They are also the only type of microbe that is capable of degrading plastics in the marine environment.
Second, the Prochlorococcus and Synechoccus species of cyanobacteria, who dominate the microbial ecology of the ocean, produce 25 percent of the world’s photosynthesized oxygen.
Third, bacterioplankton drive global biogeochemical cycles of elements through their ability to fix carbon and nitrogen, and to carry out denitrification and nitrification.
Most of the biomass (living stuff) in the ocean consists of viruses. 12 They attack and kill bacteria, archaea and other marine microbes, thus liberating the victim’s cell contents, adding to the dissolved organic carbon in the water. As important, they are able to manipulate the evolution of other microbes in the ocean. 13
Viruses are around 100 nanometers in size: (a nanometer is one millionth of a millimeter). They are generally host specific – meaning, a given virus usually affects only a certain species, or even certain kinds of cells within a species.
Also, most marine viruses are “bacteriophages” – meaning, they only infect bacteria – and are harmless to animals and plants but essential to the health of saltwater and freshwater ecosystems. 14
Unfortunately, despite improvements in microbiological research, the aquatic microbe kingdom is still poorly understood. The role and importance of viruses in the recycling of nutrients in marine ecosystems, for example, is only just coming to light. 15 16
What is the Role of Viruses in the Ocean?
Marine viruses influence biogeochemical cycles, and regulate the flow of carbon through marine food webs. In addition, viruses kill around one-fifth of the oceanic microbial biomass daily, which has a major influence on species diversity as well as nutrient and energy cycles.
Analysis of microbial food web models indicates that viral cell-bursting attacks on other microorganisms enhances the transfer of microbial biomass into the pool of dissolved organic carbon. 17
In addition, viruses are believed to regulate bacterial population explosions. For example, researchers are investigating to what extent marine cyanophages can prevent eutrophication of lakes, estuaries and coastal zones.
Finally, viruses provide key mechanisms for recycling ocean carbon and nutrients. In a process known as the viral shunt, organic molecules released from dead bacterial cells stimulate fresh bacterial and algal growth.
The Viral Shunt
As we saw, in the classical food chain, phytoplankton are eaten by zooplankton, who in turn are eaten by fish, and so on. The viral shunt (diversion) is a mechanism that diverts the flow of organic carbon (from dead microbes) out of the food chain and into the microbial loop. (It may return to the food chain in due course.) Viruses attack and destroy the living cells of bacteria, phytoplankton and microzooplankton, scattering organic matter into the water. These tiny particles of dissolved organic carbon (DOC) are readily taken up by other marine microbes, who benefit from the fast recycling of nutrients. As much as a quarter of all the carbon fixed by photosynthesizing cyanobacteria is shunted (diverted) by viruses in this manner. 18
In addition, the viral shunt helps to export carbon into the depths through the so-called biological pump. This is estimated to cause 3 billion tonnes of CO2 to be sequestered annually in the deep ocean – CO2 that would otherwise ramp up the greenhouse effect and intensify the effects of global warming.
The constant viral attacks are believed to achieve five things.
First, they kill the infected organism thus preventing it from being eaten and passed up the food chain, out of reach of the microbial population. Second, they liberate crucial nutrients – such as nitrogen and phosphorus, as well as cellular components such as amino acids and nucleic acids – making them immediately available to phytoplankton and other marine microbes, thus stimulating growth. 19
Third, the carbon-rich but less digestible cell walls of the victim fall into the depths, with less likelihood of being grazed or decomposed during their descent, and because they contain an increased proportion of carbon, they boost the efficiency of the biological pump. 20
Marine Microbes and Climate Change
In many ways, what Planet Earth will look like in 100 years depends on how marine microbes respond to a changing climate. Unfortunately, we are still at a very early stage in our understanding of how microorganisms like bacteria and viruses behave, and what drives them. New research technologies are emerging that may expedite our grasp of microbial activity, but the ocean is a big place and probing this vast reservoir of genetic and biological material is going to take a lot more time and resources. 22
In other words, we can’t predict whether viruses, for example, will exacerbate or reduce the effects of global warming on the ocean and its network of ecosystems. For example, we don’t know whether ocean warming and its effects – such as ocean deoxygenation – is likely to harm marine microbes, or whether they will adapt and prove themselves superior to other creatures.
All we can say is that marine viruses are both abundant and active enough to influence the oceans’ response to the global climate crisis. Indeed, viruses influence numerous climate-related mechanisms from the oceanic biological pump to cloud formation, although viruses themselves will not be immune to rising temperatures or to changes in ocean acidification, salinity and nutrient levels. 17
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