Microbial Ecologies: The Role of Viruses in the Marine Environment

This discussion topic submitted by doug escribano ( douglas.escribano@gs.com) at 11:00 pm on 6/8/01. Additions were last made on Friday, August 16, 2002.

Microbial Ecologies: The Role of Viruses in the Marine Environment


Technological advances often lead to new perspectives about the world in which we live. Oceanography, in particular, benefits almost daily from research that adds to our understanding of this nutrient rich and bio-diverse domain. At the beginning of the 20th Century, biological research centered on oceanic processes visible to the human eye. This limiting factor meant that most studies were based on organisms caught in dredge nets or viewed in shallow coral reefs. Smaller organisms were filtered through fine mesh nets and only what was retrieved could be examined. Today’s advances in microscopy, staining and filtration techniques offer scientists a broader methodology from which to work. One area benefiting from these innovations is the study of the marine microbial environment.

One of the most fundamental changes in scientific thought over the past 25 years has been that of the role of viruses and bacteria in the aquatic environment. Since the early 1900’s researchers were aware of the presence of viruses and bacteria in both fresh and marine waters. The basic understanding at the time concluded neither played a major role in biological processes within the ecosystem and therefore they were largely ignored. With the advent of electron microscopes and finer ceramic filters, scientists were given new opportunities to explore these microorganisms. As early as the 1970’s research began to indicate marine bacterial counts were higher then previously thought. Scientists took an interest in these findings. It was thought that something so abundant within the waters must have a more significant role.

By the late 1970’s and 80’s investigators found there were real possibilities to obtain reliable data and they began to re-examine the biodiversity of the oceans. Azam was of the first to focus on bacteria in the marine microbial environment. In 1983, he and his colleagues published a paper entitled The Ecological Role of Water-Column Microbes in the Sea. Using acridine orange direct counts and electron microscopy, they estimated bacterial biomass. The numbers varied between 1 x 104 and 5 x 106 cells/ml.1 Most of the material was free floating bacterioplankton. As with most scientific endeavors, the data only led to more questions. An offshoot of these early studies was the role of viruses in aquatic ecosystems. Bacteria are relatively small particles and do not sink out of the water column, however data showed that their numbers remained consistent. Therefore there must be something within the water column which was removing the bacteria.

By the late 1980’s and first part of the 1990’s, researchers had established a link between the bacterioplankton and nutrient cycling and carbon flow within the oceans. In his 1983 paper Azam hinted at this new direction when he used the phrase microbial loop in discussing the return of nutrients to the food chain.2 Using ultracentrifugation and 0.02um pore filters, researchers found viruses to have an even higher abundance than the bacteria. In his 1999 review article in Nature, Fuhrman states that viruses are “the most abundant biological entities” in the oceans.3 They have been found in all waters ranging from the tropics to the poles and the from the surface to the sediment. He estimated that viruses measured as high as 1010 per liter of sea water4. Today’s research continues to indicate that the microbial loop is indeed fundamental to many marine biological processes. Viruses directly impact bacterial populations, nutrient and carbon cycling and microbial genetic composition. In order to understand this role, I will limit my discussion to the biology of viruses, the microbial loop in the classic food chain and carbon flux.

Generally, viruses are defined as intracellular obligate parasites. These submicroscopic particles measure between 20-300nm. They are considerably smaller than cells and therefore cannot be viewed under traditional bright light microscopes. They have two distinct life cycles, one extracellular and one intracellular. While outside of a host cell, the virus particle is called a virion. This is essentially a genetic core surrounded by a protective protein coat called the capsid. During the extracellular stage of its natural history, the virus is metabolically inert. The intracellular form is an active parasite within the host cell. It is this form that gives viruses their most unique biological characteristic. Viruses are acellular and cannot metabolize their own energy. The virion cannot produce its own ATP. There are no molecular processes like fermentation, cellular respiration or photosynthesis. The genetic code, which is necessary for these pathways to occur, does not exist within its genome. This is why it is necessary for the virus to invade another organism. After penetrating a host cell, the virus introduces its own genome into that cell’s genetic composition. Viral genomes are small and carry only the necessary codes for viral functions, which cannot be adapted from the host organism. Once inside an organism, the virus is able to replicate using the host cells own molecular machinery.

The genetic composition of a virion is nucleic acids. These are divided in to two classes, either DNA or RNA. A third class, called retroviruses, contains both DNA and RNA but at different stages of the reproduction cycle. Retroviruses have an RNA genome in the virion but replication in the host is carried out via DNA and the enzyme reverse transcriptase. In all three groups, the genetic material can either be single or double stranded. Because the viral particle is dependent upon the host cell, the genetic make-up of the virion must match or at least be recognizable by the host organism. Penetration of the virus is achieved through a host-virus interaction between the viral particle and host cell surface. In bacteria, this is accomplished via the structure of the virus while in animals the virion usually enters the host cell by means of endocytosis.

Viruses are known to infect several types of prokaryotic cells both in Bacteria and Archea. Those parasitizing bacteria are called bacteriophages. They interact with cells by means of proteins and molecules both on the phage capsid and host’s cell wall. The structure of the bacteriophage consists of a head and a tail. The head holds the genetic material and the tail is long with fibers at its end. When a virion makes contact with a cell, the tail fibers interact with polysaccharides found on the outer layer of the host cell wall. These fibers retract allowing the tail to extend touching the outer layer. Once this is done enzymes from the tail produce a small hole in the layer allowing the viral genetic material to slip from the head into the cell.


Bacteriophages have been studied extensively. This is due in part to certain strains having small genomes and relatively simple life cycles. However there are others with more complicated natural histories. A few of the most common are: the single stranded RNA bacteriophage, MS2, the single stranded DNA, M13 and the double stranded DNA viruses, Lambda and T4. Bacteriophage Lambda is one of the most studied viruses providing a good model for the general infection and replication mechanisms used by the mature viral particle.

Lambda is considered a temperate virus, which is one that does not necessarily destroy its host when the virion coops the host’s cellular machinery. This strain can follow one of two pathways once the DNA material has been injected into the host cell. They are either the lysogenic or lytic pathways. Lysogeny pathway allows for cell division and normal cell growth. However, the virus integrates its DNA in to the host genome and therefore viral DNA is being replicated for another generation. These cells continue to divide and maintain growth, however under the certain conditions they can be induced to move into the other pathway. This is one impact viruses have on marine environments, they alter the genetic composition of the bacterioplankton.

The lytic pathway is reproduces mature viral particles for release into the environment. Once DNA material is injected into the host cell, molecular changes begin to occur. The biochemistry of the cell is altered to favor the virus. Early on viral enzymes are produced. These so-called early proteins are necessary for replication of viral nucleic acids. Once these have been made the genetic material is replicated. The following step involves the synthesis of the protein coat. Next, the DNA and the capsid are assembled and packaged. At this point, the host cell has served it purpose. Cell lysis releases the virus back in to the environment so that they can again infect another host organisms.

The classic food web of the ocean has been stated to be one based on trophic levels in which species or groups of species feed on one or more species from a lower level. This gives a pyramid form to the picture with the most abundant organisms at the base while moving gradually toward the tip where the consummate predators such as sharks are found. The efficiency of this pyramid is such that it takes less energy to produce the smaller organisms than it does the larger ones. Therefore much of the energy which is produced at one level is lost to the next higher level. Energy is lost at each step and it this reason why the pyramid gets smaller at the top. There is less energy available at the top to produce the small abundant numbers seen at the bottom.

In the water column, one can measures productivity of the organisms found within the food web. The calculation for this is often expressed terms of the amount of living tissue produced in a given amount of time.5 As an equation this is expressed as grams of carbon produced per day in a column of water intersecting one square meter of sea surface or (gC/m2/day).6 As we well see the majority of the biomass of the oceans is found at the bottom of the trophic levels. The organisms found here are considered the basis of the marine food web. They play an important role in nutrient and carbon cycling.

The primary producers within the marine environment are those that metabolize via photosynthesis. These organisms use light energy and inorganic material to incorporate CO2 into their cellular composition (there are groups found in deep ocean trenches which use chemicals rather then light as their energy source). Oxygen is their primary by-product. However during photosynthesis, carbon dioxide and water combine to produce organic carbohydrates. These become available to higher levels of the food web either by being eaten or being released back into the water column as dissolved organic material. In a typical ocean ecosystem, the productivity of this base group is more then all of the other organisms. Organisms, which are self-feeding because they make their own organic material from the inorganic are called autotrophs.

In general microorganisms in the ocean are broken down by size categories. These include: femtoplankton (viruses) at approximately 0.01-.02um, picoplankton (including bacteria, Archaea and eukaryotes) at approximately 0.3-2.0um, nanoplankton (protists-flagellates) at approximately 2-20um, microplankton (microalgae) at approximately 20-200um and finally macroplankton at approximately 200um or larger.7

Phytoplankton are primary producing autotrophs in the oceans. They are unicellular algal organisms (protists) usually suspended in the water column. This means that these microbes are not capable of independent movement. They depend upon wave action for moving them through the water column. In part it is this water movement which keeps these small particles from sinking to the bottom where they would be unable to use the sunlight. Viruses are non-motile microorganisms as well. In the oceans, viruses are suspended in the water column and passively wait until making contact with a bacteriophage host. Viruses are heavier then seawater but are kept suspended in the water column by wave action.

One dominant class of phytoplankton is the Diatoms. These can be either single cellular or form cell chains. Their size ranges from nanoplankton to microplankton. They are found in both temperate and polar waters. Diatoms have an outer cell wall made of silica. This layer is called the frustule. Each species of diatoms has a different frustule structure making them easily identifiable. These microbes have an interesting evolutionary history. The silica shell is preserved and leaves a fossil record.

Another class of phytoplankton is the Dinoflagellates. These flagellated unicellular microbes are found in subtropical and tropical waters, but may also be found in temperate zones in the summer and early autumn months. Their size ranges from nanoplankton to microplankton. A unique characteristic of these protists is that they have two flagellum. One is transverse and encircles the body, while the other is longitudinal and perpendicular to the first. Both are attached to the cell wall at the same point. This gives dinoflagellates a distinctive spiral swimming motion. They are biologically important because they are primary producers, however they are also know for the phenomena called red tide. Under certain conditions and when large numbers are present, these phytoplankton produce a reddish hue to the water. They also excrete a toxin that can have detrimental effects to the ecosystem. One possible explanation for these tides is the introduction of excess nutrients such as phosphates in to the environment—often by humans.

A third class is the Cyanobacteria. These unicellular microbes are found throughout the oceans. They are considered to be one of the oldest organisms on the planet. Cyanobacteria have a fossil record that goes back 3.5 million years. It is believed that these early bacteria through photosynthesis oxygenated our atmosphere. These microorganisms are related to toady's plants as well. Chloroplasts found in modern plants are believed to have been cyanobacteria. In the oceans, they play a role in the fixation of nitrogen. During this process, gaseous nitrogen is converted to ammonium ion which becomes available for incorporation in to amino acids and proteins.

The other group of microorganisms found in the food chain is zooplankton which is comprised of non-photosynthetic protists and animals. These organisms can be single cellular or multi-cellular and include small animals such as fish larvae. Usually these organisms are capable of some motility, but they are affected by water turbulence. Zooplankton are considered heterotrophic because they consume organic material. Within this group one finds the heterotrophic bacteria. Bacterioplankton are prokaryotic microbes dominated by gram-negative bacteria. These microorganisms catabolize carbon molecules during respiration.8 In the photic zone, this heterotrophic bacteria is thought to represent approximately 70% of the living carbon.9

The oceanic food web is considered to be one of the most complex systems because of the various cycles flowing through it. This ecosystem is a storehouse for the various chemicals from which we are made. In the ocean there is carbon, nitrogen, oxygen, sulfur and others. These chemicals flow through the food chain, moving from the plankton to small vertebrates and invertebrates on to larger organisms, finally reaching the largest of marine mammals. Along the way, organic material made by the primary producers is transferred to the next level. The first law of thermodynamics states that energy is neither created nor destroyed. Therefore, this constant nutrient and carbon cycling in the oceans becomes a fundamental player in biological processes. The process is a continual, however some organic matter is removed from the food chain when it is incorporated in petrified wood or fossilized bones. However, these processes take millions of years while daily production of matter by the primary producers is huge.

In the microbial loop, phytoplankton such as diatoms and dinoflagellates begin the process when they use photosynthesis for their metabolism. These microbes are then eaten by organisms in the next level which includes the heterotrophic bacterioplankton. At this point, there are two pathways in which the organic material can be used If the bacterioplankton is eaten by a consumer in the next level, the carbon continues on a line through the food pyramid, however if the bacterioplankton is infected by a viruses, during the lytic cycle, the carbon material is returned to the microbial loop when the cell lysises. The carbon is returned in the form of dissolved organic material.

In the past, it was thought that carbon did not spill out of the food chain and therefore there was little dissolved organic material available to microbes. This is another reason for the microbial environment to be largely ignored until 25 years ago.. It was originally thought that grazing within the food chain by higher levels returned some carbon material to the lower levels. Previous thought also suggested that bacteria only played a role as decomposer within the environment. Once there was an understanding that carbon and nutrients, such as nitrogen and phosphorous, were being returned to the microbial loop, researchers realized that there was a much broader processes involved in the oceans. Researchers found that particulate organic carbon and dissolved organic carbon both play an important role in the microbial ecology of the seas. Heterotrophic microorganism primarily consumes both. Within an aquatic system, much of the dissolved organic carbon remains within the microbial loop. This process can repeat several times before the carbon leaves the microbial loop. It is still not completely known what the fate of all the cellular material is when a cell is destroyed by a virus. Not all the carbon is released in the form of dissolved organic matter. Larger components like the lipid bilayer and cell wall are probably transferred to the next level. However, this means that there is a certain level of carbon not being removed from the immediate environment. The particulate organic carbon can be transferred to the next trophic level. Sherr states that the microbial loop serves as the primary pathway for the regeneration of organic nitrogen and phosphorus and as a shunt of carbon and energy from the main phytoplankton-based food web.9

This is important because it directly impacts the primary producers. It has been suggested that “viral lysis leads to an increase in bacterial production but a decrease in the transfer of carbon to higher trophic levels”. 10 Using a food model, Wilhelm and Suttle found that 6-26% of photosynthetically fixed organic carbon was recycled back into the microbial loop.11 Fuhrman found in one model a food web with a 50% bacterial mortality due to viruses, had a 27% bacterial respiration and production rate and a 37% less bacterial grazing rate by protists.12 The overall effect means there is a reduction in macrozooplankton when compared to systems in which there were no viruses.

Today, new research indicates that both bacteria and viruses are fundamental to our oceans. Viruses are not longer viewed as static but seen as dynamic players within the microbial ecology of the oceans. By means of cell lysis, viruses return carbon to the ocean which was derived from photosynthesis. The particles also have a function in the control of bacterial blooms and altering the genetic composition of its host. The field of marine microbial ecologies is just beginning to come into its own with newer technologies. More research is required to fully understand the processes that occur in the microbial loop. However, viruses certainly play a central role and there are many questions remaining to be answered.

Endnotes:
1. F. Azam et al. The Ecological Role of Water-Column Microbes in the Sea. Marine Ecology- Progress Series. Vol. 10, 1983, p. 258.

2. Ibid., page 260.

3. Jed A. Fuhrman. Marine Viruses and their Biogeochemical and Ecological Effects. Nature. Vol. 399, June 10, 1999, p. 541.
4. Ibid., page 541.

5. Jeffrey S. Levinton, Marine Biology, Function, Biodiversity, Ecology. New York: Oxford University Press, 1995, p. 194.

6. Ibid., p. 194.

7. Evelyn and Barry Sherr. Marine Microbes. In Microbial Ecology of the Oceans, ed. David Kirchman, New York: Wiley & Sons, Inc. p. 13.

8. Ibid., p. 19

9. Steven W. Wilhelm and Curtis A. Suttle, Viruses and Nutrient Cycles in the Sea. BioScience. Vol. 49, October 1999, p. 781.

10. Ibid., p. 785

11. Ibid., p. 785

12. Jed A. Fuhrman, Impact of Viruses on Bacterial Processes. In Microbial Ecology of the Oceans, ed. David Kirchman, New York: Wiley & Sons, Inc. p. 340.


Bibliography:
Azam, F., Microbial Control of Oceanic Carbon Flux: The Plot Thickens, Science, 280 (1998): 694-696.
Azam, F., Fenchel,T., Field, J. G., Meyer-Reil, R. A. and Thingstad, T. F., The Ecological Role of Water Column Microbes in the Sea, Marine Ecology Progress Series 10 (1983): 257-263.
Bergh, O., Borscheim, K. Y., Bratbak, G. and Heldal, H., High Abundance of Viruses found in Aquatic Environments, Nature 340 (1989): 467-468.
Crawford, Dorothy, H. The Invisible Enemy: A Natural History of Viruses. Oxford: Oxford University Press, 2000.
Fuhrman, Jed, A. and Noble, P. T., Viruses and Protists Cause Similar Bacterial Mortality in Coastal Sea Waters, Limnology Oceanography 40 no. 7 (1995): 1236-1242.
Fuhrman, Jed, A., Marine viruses and their Biogeochemical and Ecological Effects, Nature 399 (10 June 1999): 541-548.
Fuhrman, Jed A., Impact of Viruses on Bacterial Processes. In Microbial Ecology of the Oceans, edited by David L. Kirchman, New York: Wiley-Liss, Inc. 2000.
Gonzalez, J. M. and Suttle, C. A., Grazing by Marine Nanoflagellates on Viruses and Virus-sized Particles-Ingestion and Digestion, Marine Ecology Progres. Series 94 no.1 (1993): 1-10.
Heldal, M. and Bratbak, G., Production and Decay of Viruses in Aquatic Environments, Marine Ecology Progres. Series 72 (1991): 205-212.
Kirchman, D. L., Oceanography: Microbial Ferrous Wheel, Nature 383 (6 May 1998): 303-304.
Levinton, Jeffrey, S. Marine Biology: Function, Biodiversity, Ecology. Oxford: Oxford University Press, 1995
Sherr, Evelyn and Barry, Marine Microbes an Overview. In Microbial Ecology of the Oceans, edited by David L. Kirchman, New York: Wiley-Liss, Inc., 2000
Valiela, Ivan. Marine Ecological Processes. New York: Springer, 1995.
Waller, Geoffrey (ed.), SeaLife: A Complete Guide to the Marine Environment. Washington DC, Smithsonian Institution Press, 1996.
Wilhelm, Steven, W. and Suttle, Curtis, A., Viruses and Nutrient Cycles in the Sea. BioScience, 49 no. 10 (1999): 781-788


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