Do Viruses Control the Oceans?

Natural History, Feb, 1999 by Curtis A. Suttle

Infection may be the spice of planktonic life.

The thousands of pinpoints of light against the blackness made it easy to imagine I was in a spaceship traveling through the far reaches of the galaxy. What I was looking at were not stars, however, but the DNA of viruses in seawater, magnified a thousand times and glowing under the blue light of the epifluorescence microscope. Observations on the abundance and dynamics of such virus particles have been changing our understanding of the world's oceans.

That the oceans teem with viruses was discovered only a decade ago by Lita Proctor, a graduate student working in microbial ecologist Jed Fuhrman's laboratory at the State University of New York at Stony Brook, and--at virtually the same time--by a group working with Gunnar Bratbak, professor of microbiology at the University of Bergen in Norway. I was doing postdoctoral work in Fuhrman's laboratory at the time and had a chance to witness the unfolding drama. These researchers were finding that each teaspoonful of seawater typically contains about 10 to 100 million viruses, ten times more than the next most numerous inhabitants of the typical teaspoonful: bacteria (also known as bacterioplankton). Electron microscopy revealed that viruses are not only abundant but also diverse in appearance. Many of the small ones resemble lunar landers, with polygonal "heads" and little jointed "legs" attached to "tails"; others are much larger and have no tails. Each virus, consisting of genetic material encapsulated in a protein shell, is so small that it would take about 23 billion of them--or about four times the number of people on the earth--to make a visible particle.

Once it was demonstrated that viruses are an enormous presence in the sea, the next step was to assess their effect on marine ecosystems. In 1988 I began to explore these issues at the University of Texas along with Amy Chan, my research associate and spouse, and Matthew Cottrell, then a first-year doctoral student. Since 1996 Amy and I have conducted similar research at the University of British Columbia, in Vancouver. A key question for us has been the viruses' role in the life and death of bacterioplankton, phytoplankton, and microzooplankton--the one-celled organisms that drift with the currents on the surface of the open ocean. Staple items of the food web, plankton are the producers and recyclers of most of the energy that flows through oceanic ecosystems.

Viruses are not alive, in the sense that they have no metabolism when outside a host, and they can reproduce only by infecting living organisms. When a virus injects its DNA into a cell, it hijacks that cell's replication machinery and produces scores or hundreds of new viral particles. These rupture the host and are released into the environment to find new victims. In a multicellular animal such as a human, a viral invasion does not always result in serious illness, much less death, but for a single-celled planktonic organism, the process of viral replication is generally lethal.

Some viruses, known as lysogenic phages, add a twist to this life cycle. Once they insert their DNA into the host cell's genetic material, they do not immediately use the host's machinery to replicate themselves, but their genes are duplicated each time the host cell divides. Only an environmental cue--such as exposure to sunlight or a sudden temperature change--will trigger their own replication process. At that point, however, the virus leaves the host, sometimes absconding with some of the host's genetic material. Now the virus becomes a genetic engineer: when it infects its next host, it does so with a combination of its own and the previous host's DNA. In this way, a virus may shunt DNA from individual to individual and between populations. (Fortunately, most viruses are limited to particular hosts, so this kind of commerce is limited to a few closely related species--bacteria of a single genus, for example.)

What we didn't know when we began our work was the extent of viral effects on sea life. We knew the marine viruses were abundant, but that did not necessarily mean they had a great impact. Many viruses are extremely stable in water, so it was possible that the ones we were seeing in seawater had been drifting around for years without infecting other organisms. If so, a very high concentration of viruses was being maintained by a very low rate of infection. Another possibility was that a great proportion of the viruses we were observing had been rendered harmless, owing to damage from exposure to sunlight or from other unknown causes. A third possibility was what we were expecting: that their abundance meant they were constantly infecting other organisms.

We decided to pursue a hunch that many of the viruses were pathogens of phytoplankton--photosynthesizing organisms such as cynobacteria, small flagellates, and other unicells that form the base of the food web in the ocean. Other researchers had primarily focused on non-photosynthesizing bacteria as potential host organisms, but a number of observations suggested that phytoplankton were also important targets of infection. For one, viruslike particles had been found in many different types of phytoplankton, although with little direct evidence of actual viral infection. And researchers Jolie Mayer and Max Taylor, of the University of British Columbia, had managed to isolate a virus from infected phytoplankton in the late 1970s. Finally, anecdotal reports in scientific journals had described the sudden disappearance of phytoplankton blooms from various areas of the ocean's surface.