What is a virus?
Viruses are parasites of living cells which invade cells and then use their biological machinery to propagate. Most viruses in the ocean consist of nucleic acids surrounded by a protein coat (called a capsid). Viruses are thought to have appeared several times during the evolution of cellular organisms as suggested by the type (DNA vs RNA) or structure of the nucleic acid (double-strand vs single strand; sense vs antisense). In marine environments, they are more numerous than the most abundant cell types, the prokaryotes. Prokaryotes are single-celled organisms without a nucleus and are now considered to consist of the two so-called domains of life, Bacteria and Archaea. Viruses are a major factor for the mortality of marine prokaryotes.
What organisms do they infect?
Most viruses in the ocean are thought to infect prokaryotes. They are typically DNA-containing viruses and, if they infect bacteria, are called bacteriophages or “phages” for short. Most phages, at least in the surface ocean, belong to three phage groups of the tailed phages. Some of these phages look like moon landers. The morphological diversity of the phages is high: they vary in capsid size as well as tail length and structure and can have appendices. In the deep ocean around hydrothermal vents spindle forms are found, which are typical for some groups of viruses infecting Archaea. In surface waters, very large viruses can be found, often with capsid diameters of 200 - 400 nm (0.000002 - 0.000004 mm). These viruses are larger than some prokaryotic cells. They probably infect single-celled photosynthetic organisms (phytoplankton) of the third domain of life, the Eukarya (cells with a nucleus). Even larger virus-like particles (700 nm) have been found in the food vacuoles of radiolarians (skeleton-forming protists). Viruses also infect metazoans and benthic plants. For example, some epidemic diseases of fish and seals have been caused by viruses. It is likely that viruses infect all cellular organisms in the ocean, from prokaryotes to whales.
The genetic diversity of viruses
Only a tiny portion of the viruses from the ocean have been characterized. One of the reasons for that is that it was only 15-20 years ago that scientists realized that viruses play a key role in the functioning of the ocean. Another reason is that for a characterization of viruses, their host or host cells have to be available. This is a problem, since most prokaryotes have not been cultivated in the controlled environment of a laboratory. However, more emphasis is currently put into isolation of so called virus-host systems.
To circumvent the isolation and cultivation problems, cultivation-independent methods have been developed. These are based on the detection of specific genes that are found exclusively in viruses. A major focus in this area has been phages infecting a group of photosynthesizing bacteria, the cyanobacteria (formerly known as blue-green algae). Cyanobacteria can contribute significantly to photosynthetic carbon fixation (primary production). Using sequence analysis, many new types of these phages (called cyanophages) have been detected. Some of these sequences seem to be specific for environments such as estuaries or the open ocean. Also, a specific depth distribution in the water column is found. For example, specific sequences of cyanophages could only be detected in the deep chlorophyll maximum (DCM), a Chlorophyll-rich layer closely associated to the thermocline (ca 75 to 200 m depth). Many new sequences from uncultivated algal viruses (Phycodnaviridae) could be found as well. Sequence analysis and isolation of viruses showed that some viruses have a cosmopolitan distribution, whereas others seem have a more restricted geographical range.
Recently, attempts have been made to sequence all the genes from all of the viruses from environmental samples. Using this community or metagenomic approach, between 370 and 7,100 viral types have been detected in two coastal samples. These DNA viruses mainly infected prokaryotes. RNA virus metagenomics showed there is also a large, previously unknown diversity of RNA viruses in the coastal ocean. The RNA viruses most likely infect eukaryoytes. Metagenomics suggest that viruses represent the largest unknown sequence space in the ocean. It has also been suggested based on metagenomics data that the coastal marine sediments are the most diverse biological system characterized so far. This means that for the vast majority of the sequences, it is not known what they are encoding for.
Recent studies have revealed a surprising functional diversity of viruses and the presence of evolution of specific viral genes. For example, viruses have genes to repair DNA damage such as caused by sunlight. Homologs of these repair genes were found in very diverse viruses such as the T4 phage infecting Escherichia coli and an algal virus infecting the symbiotic algae Chlorella. However, this gene has not been found in the genome of a cellular organisms. Cyanophage can also carry genes involved in the process of photosynthesis (which is normally attributed to only algae and plants). This is surprising, since viruses have no metabolism of their own. From observations in lab studies, it appears that these cyanophage-encoded photosynthesis genes force the infected host cell to continue with photosynthesis until shortly before cell lysis. This probably increases the energy available within the infected cell so that a maximum of new cyanophage particles can be produced. Thus, viruses do interfere with host functions in a much more sophisticated way than previously thought.
Virus life cycles
Viruses have several different life (or replication) cycles. The two most dominant are the lytic and the lysogenic (latent) cycle. Lytic (or virulent) viruses infect a cell (or tissue), replicate (i.e. make new viruses) and are released by lysis the host cell. Temperate viruses infect the host and the viral DNA stays within the host cell, often in the host genome. It is said that they lysogenize the host. For eukaryotes typically the term latency is used. The viral genome replicates along with the host genomes, until some factors, such as DNA damage, induce the lytic cycle. For prokaryotes in the ocean, it has been suggested that in nutrient-rich waters (characterized by a high abundance of hosts) lytic phages dominate, whereas in nutrient-poor waters (characterized by a low abundance of hosts), lysogeny dominates.
Effect of viruses on host diversity
It is well established, albeit not fully appreciated, that the activity of phages has a very strong influence on the diversity and distribution of bacteria. Viruses play a role in the evolution of the host by virus-mediated gene transfer to hosts. However, they also play a role in the maintenance of host diversity at ecological scales. Experimental data have shown that lytic viruses can affect the diversity of host communities of Bacteria and Archaea. Conceptual and mathematical models suggest that viruses can influence the winner in competitions for nutrients. In this scenario, once a microbe becomes dominant, the increase in abundance increases its contacts with viruses leading to significant increases in infection and subsequent lysis, which then control its abundance. This model has been called the ‘kill the winner’ hypothesis. As a consequence, viruses may sustain a high population diversity amongst their hosts by controlling the growth of organisms that would extensively proliferate due to advantages in nutrient acquisition. This would allow for the survival of less competitive but virus-resistant microbes.
Effect of virus on environmental chemistry
Viruses in marine environments also play many important roles in the ecology of these ecosystems. Perhaps one of their most important roles is in system biogeochemistry, as through the process of infecting and lysing their hosts, viruses convert both macronutrients (nitrogen and phosphorus) as well as micronutrients (e.g., iron) from particulate forms to dissolved forms that are then available for actively growing phytoplankton and bacteria to consume. Through this process viruses work not only to recycle these nutritional elements, but also to return these elements to the water column in chemical compounds that may not be typically produced by other processes. When bacteria consume organic material, they often remineralise nutrients as inorganic forms back into the water column. However, when viruses lyse bacteria, the nutrients are released in the water column within the organic compounds which were present in the cell. These organically-complexed nutrients released to the marine community during virus lysis therefore need to be assimilated into cells by different biochemical pathways than those released during the remineralization of organic material. As such this process may alter the selective pressures on the marine microbial community in terms of having the necessary pathways to assimilate the chemical forms these obligate nutrients. Such a change in selective pressure will also affect the community composition of the plankton.
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