A Planet of Viruses - Carl Zimmer (2011)

EVERYWHERE, IN ALL THINGS

The Infected Ocean

Marine Phages

Some great discoveries seem at first like terrible mistakes.

In 1986 a graduate student at the State University of New York at Stony Brook named Lita Proctor decided to see how many viruses there are in seawater. At the time, the general consensus was that there were hardly any. The few researchers who had bothered to look for viruses in the ocean had generally found only a scarce supply. Most experts believed that the majority of the viruses they did find in sea water had actually come from sewage and other sources on land.

But over the years, a handful of scientists had gathered evidence that didn’t fit neatly into the consensus. A marine biologist named John Sieburth had published a photograph of a marine bacterium erupting with new viruses, for example. Proctor decided it was time to launch a systematic search. She traveled to the Caribbean and to the Sargasso Sea, scooping up seawater along the way. Back on Long Island, she carefully extracted the biological material from the seawater, which she coated with metal so that it would show up under the beam of an electron microscope. When Procter finally looked at her samples, she beheld a world of viruses. Some floated freely, while others were lurking inside infected bacterial hosts. Based on the number of viruses she found in her samples, Proctor estimated that every liter of seawater contained up to one hundred billion viruses.

Proctor’s figure was far beyond anything that had come before. It would have surprised few scientists if she had turned out to have added on a few extra zeroes by accident. But when other scientists carried out their own surveys, they ended up with similar estimates. Scientists came to agree that there are somewhere in the neighborhood of 1,000,000,000,000,000,000,000,000,000,000 viruses in the ocean.

It is hard to find a point of comparison to make sense of such a huge number. Viruses outnumber all other residents of the ocean by about fifteen to one. If you put all the viruses of the oceans on a scale, they would equal the weight of seventy-five million blue whales. And if you lined up all the viruses in the ocean end to end, they would stretch out past the nearest sixty galaxies.

These numbers don’t mean that a swim in the ocean is a death sentence. Only a minute fraction of the viruses in the ocean can infect humans. Some marine viruses infect fishes and other marine animals, but by far their most common targets are microbes. Microbes may be invisible to the naked eye, but collectively they dwarf all the ocean’s whales, its coral reefs, and all other forms of marine life. And just as the bacteria that live in our bodies are attacked by phages, marine microbes are attacked by marine phages.

When Felix d’Herelle discovered the first bacteriophage in French soldiers in 1917, many scientists refused to believe that such a thing actually existed. A century later, it’s clear that Herelle had found the most abundant life form on Earth. Ever since Proctor’s discovery of the abundance of marine viruses, scientists have been documenting their massive influence on the planet. Marine phages influence the ecology of the world’s oceans. They leave their mark on Earth’s global climate. And they have been playing a crucial part in the evolution of life for billions of years. They are, in other words, biology’s living matrix.

Marine viruses are powerful because they are so infectious. They invade a new microbe host ten trillion times a second, and every day they kill about half of all bacteria in the world’s oceans. Their lethal efficiency keeps their hosts in check, and we humans often benefit from their deadliness. Cholera, for example, is caused by blooms of waterborne bacteria called Vibrio. But Vibrio are host to a number of phages. When the population of Vibrio explodes and causes a cholera epidemic, the phages multiply. The virus population rises so quickly that it kills Vibrio faster than the microbes can reproduce. The bacterial boom subsides, and the cholera epidemic fades away.

Stopping cholera outbreaks is actually one of the smaller effects of marine viruses. They kill so many microbes that they can also influence the atmosphere across the planet. That’s because microbes themselves are the planet’s great geoengineers. Algae and photosynthetic bacteria churn out about half of the oxygen we breathe. Algae also release a gas called dimethyl sulfide that rises into the air and seeds clouds. The clouds reflect incoming sunlight back out into space, cooling the planet. Microbes also absorb and release vast amounts of carbon dioxide, which traps heat in the atmosphere. Some microbes release carbon dioxide into the atmosphere as waste, warming the planet. Algae and photosynthetic bacteria, on the other hand, suck carbon dioxide in as they grow, making the atmosphere cooler. When microbes in the ocean die, some of their carbon rains down to the sea floor. Over millions of years, this microbial snow can steadily make the planet cooler and cooler. What’s more, these dead organisms can turn to rock. The White Cliffs of Dover, for example, are made up of the chalky shells of single-cell organisms called coccolithophores.

Viruses kill these geoengineers by the trillions every day. As their microbial victims die, they spill open and release a billion tons of carbon a day. Some of the liberated carbon acts as a fertilizer, stimulating the growth of other microbes, but some of it probably sinks to the bottom of the ocean. The molecules inside a cell are sticky, and so once a virus rips open a host, the sticky molecules that fall out may snag other carbon molecules and drag them down in a vast storm of underwater snow.

Ocean viruses are stunning not just for their sheer numbers but also for their genetic diversity. The genes in a human and the genes in a shark are quite similar—so similar that scientists can find a related counterpart in the shark genome to most genes in the human genome. The genetic makeup of marine viruses, on the other hand, matches almost nothing. In a survey of viruses in the Arctic Ocean, the Gulf of Mexico, Bermuda, and the northern Pacific, scientists identified 1.8 million viral genes. Only 10 percent of them showed any match to any gene from any microbe, animal, plant, or other organism—even from any other known virus. The other 90 percent were entirely new to science. In 200 liters of seawater, scientists typically find 5,000 genetically distinct kinds of viruses. In a kilogram of marine sediment, there may be a million kinds.

One reason for all this diversity is that marine viruses have so many hosts to infect. Each lineage of viruses has to evolve new adaptations to get past its host’s defenses. But diversity can also evolve by more peaceful means. Temperate phages merge seamlessly into their host’s DNA; when the host reproduces, it copies the virus’s DNA along with its own. As long as a temperate phage’s DNA remains intact, it can still break free from its host during times of stress. But over enough generations, a temperate phage will pick up mutations that hobble it, so that it can no longer escape. It becomes a permanent part of its host’s genome.

As a host cell manufactures new viruses, it sometimes accidentally adds some of its own genes to them. The new viruses carry the genes of their hosts as they swim through the ocean, and they insert them, along with their own, into the genomes of their new hosts. By one estimate, viruses transfer a trillion trillion genes between host genomes in the ocean every year.

Sometimes these borrowed genes make the new host more successful at growing and reproducing. The success of the host means success for the virus, too. While some species of viruses kill Vibrio, others deliver genes for toxins that the bacteria use to trigger diarrhea during cholera infections. The new infection of toxin-carrying viruses may be responsible for new cholera outbreaks.

Thanks to gene borrowing, viruses may also be directly responsible for a lot of the world’s oxygen. An abundant species of ocean bacteria, called Synechococcus, carries out about a quarter of the world’s photosynthesis. When scientists examine the DNA of Synechococcus samples, they often find proteins from viruses carrying out their light harvesting. Scientists have even found free-floating viruses with photosynthesis genes, searching for a new host to infect. By one rough calculation, 10 percent of all the photosynthesis on Earth is carried out with virus genes. Breathe ten times, and one of those breaths comes to you courtesy of a virus.

This shuttling of genes has had a huge impact on the history of all life on Earth. It was in the oceans that life got its start, after all. The oldest traces of life are fossils of marine microbes dating back almost 3.5 billion years. It was in the oceans that multicellular organisms evolved; their oldest fossils date back to about 2 billion years ago. In fact, our own ancestors did not crawl onto land until about 400 million years ago. Viruses don’t leave behind fossils in rocks, but they do leave marks on the genomes of their hosts. Those marks suggest that viruses have been around for billions of years.

Scientists can determine the history of genes by comparing the genomes of species that split from a common ancestor that lived long ago. Those comparisons can, for example, reveal genes that were delivered to their current host by a virus that lived in the distant past. Scientists have found that all living things have mosaics of genomes, with hundreds or thousands of genes imported by viruses. As far down as scientists can reach on the tree of life, viruses have been shuttling genes. Darwin may have envisioned the history of life as a tree. But the history of genes, at least among the ocean’s microbes and their viruses, is more like a bustling trade network, its webs reaching back billions of years.

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