During a single day, in the placid waters of a pond, a million virus particles could enter a single-celled organism known for the tiny hairs, or cilia, that propel it through those waters.
For the past three years, John DeLong of the University of Nebraska-Lincoln has been delving into a potentially game-changing secret: Those virus particles aren’t just a source of infection, they’re also nutrition.
In a Pac-Man twist, DeLong and his colleagues discovered that a species of Halteria, microscopic ciliates that inhabit freshwater around the world, can eat large amounts of infectious chloroviruses that share its aquatic habitat. For the first time, the team’s lab experiments have also shown that a diet based solely on viruses, which the team calls “virovoria,” is sufficient to fuel an organism’s physiological and even population growth.
Chloroviruses, a career-defining discovery by Nebraska’s James Van Etten, are known to infect microscopic green algae. Eventually, the invading chloroviruses burst their single-celled hosts like balloons, spilling carbon and other vital elements into the open sea. That carbon, which could have gone to the tiny creatures’ predators, is sucked up by other microorganisms, a grim recycling program in miniature and seemingly in perpetuity.
“That’s really keeping carbon low in this kind of microbial soup layer, preventing herbivores from taking energy up the food chain,” said DeLong, an associate professor of biological sciences at Nebraska.
But if ciliates eat those same viruses for dinner, then the virovory could be counteracting the carbon recycling that viruses are known to perpetuate. It’s possible, DeLong said, that virovory is helping carbon escape from the dregs of the food chain, giving it upward mobility that viruses otherwise suppress.
“If you multiply a crude estimate of how many viruses there are, how many ciliates there are, and how much water there is, you get this massive amount of energy movement (up the food chain),” said DeLong, who estimated that ciliates in a small pond they can eat 10 trillion viruses a day. “If this is happening on the scale that we think it could be, it should completely change our view of the global carbon cycle.”
‘No one noticed’
DeLong was already familiar with the ways that chloroviruses can become entangled in a food web. In 2016, the ecologist teamed up with Van Etten and virologist David Dunigan to show that chloroviruses gain access to algae, which are normally enclosed in a genus of ciliates called Paramecia, only when small crustaceans eat the Paramecia and excrete the algae. just exposed.
That finding put DeLong in “a different headspace” when it came to thinking about and studying viruses. Given the sheer abundance of viruses and microorganisms in the water, he thought it inevitable that even infection aside, the former would sometimes finish within seconds.
“It seemed obvious that everyone has to have virus in their mouth all the time,” he said. “It seemed like it had to be happening, because there’s so much in the water.”
So DeLong dove into the research literature, intending to surface any studies on aquatic organisms eating viruses and, ideally, what happened when they did. He got away with very little. One study, from the 1980s, reported that single-celled protists were capable of consuming viruses, but went no further. A handful of papers from Switzerland later showed that protists appeared to be removing viruses from sewage.
“And that was it,” DeLong said.
There was nothing about the potential consequences for the microorganisms themselves, let alone the food webs or ecosystems to which they belonged. That surprised DeLong, who knew that viruses were built not only on carbon, but also on other elemental building blocks of life. They were, hypothetically at least, anything but junk food.
“They’re made of really good stuff: nucleic acids, lots of nitrogen and phosphorus,” he said. “Everything should want to eat them.
“So many things will eat anything they can get their hands on. Surely something would have learned to eat these really good raw materials.”
As an ecologist who spends much of his time using mathematics to describe predator-prey dynamics, DeLong wasn’t entirely sure how to investigate his hypothesis. Ultimately, he decided to keep it simple. First, he would need some volunteers. He drove to a nearby pond and collected samples of the water. Back in his lab, he corralled all the microorganisms he could handle, regardless of species, into droplets of water. Finally, he added generous amounts of chlorovirus.
After 24 hours, DeLong searched the droplets for a sign that some species seemed to be enjoying the company of the chlorovirus, that even one species was treating the virus less as a threat than as a snack. At Halteria he found it.
“At first, it was just a suggestion that there were more of them,” DeLong said of the ciliates. “But then they were big enough that you could grab some with a pipette tip, put them in a clean drop, and count them.”
The number of chloroviruses was plummeting up to 100 times in just two days. The Halteria population, with nothing to eat except the virus, was growing on average about 15 times over that same time period. Halteria deprived of the chlorovirus, meanwhile, was not growing at all.
To confirm that Halteria was actually consuming the virus, the team labeled some of the chloroviruses dna with a green fluorescent dye before introducing the virus to the ciliates. Sure enough, the ciliated equivalent of a stomach, its vacuole, soon glowed green.
It was unmistakable: the ciliates were eating the virus. And that virus was sustaining them.
“I was calling out to my co-authors: ‘They grew up! We did it!’” DeLong said of the findings, now detailed in the Proceedings of the National Academy of Sciences. “I’m excited to be able to see something so fundamental for the first time.”
DeLong was not done. The mathematical side of him wondered if this particular predator-prey dynamic, strange as it seemed, might share common ground with the more pedestrian pairings he was used to studying.
He began by charting the decline of the chloroviruses against the growth of Halteria. That relationship, DeLong found, generally fits with those that ecologists have observed between other microscopic hunters and their hunted. Halteria also converted about 17% of the consumed chlorovirus mass into new mass of its own, right in line with the percentages seen when paramecia eat bacteria and millimeter-long crustaceans eat algae. Even the rate at which ciliates feed on the virus and the approximately 10,000-fold disparity in their sizes are consistent with other studies of aquatic cases.
“I was motivated to figure out if this was weird or not, or if it fit,” DeLong said. “This is not unusual. It’s just that no one noticed.”
Since then, DeLong and his colleagues have identified other ciliates that, like Halteria, can thrive on eating only viruses. The more they discover, the more likely it seems that the virovorium may be occurring in the wild. It’s a perspective that fills the ecologist’s head with questions: How might it shape the structure of food webs? The evolution and diversity of species within them? Its resilience in the face of extinctions?
Once again though, he has chosen to keep it simple. As soon as the Nebraska winter subsides, DeLong will head back to the pond.
“Now,” he said, “we have to find out if this is true in nature.”