The seething, microbe-rich hot springs of Yellowstone National Park are a model of the conditions in which life emerged on early Earth, many researchers think. Now, a study of one Yellowstone hot spring suggests so-called “giant viruses” played a key role in those primordial ecosystems and may have helped drive early steps in evolution.
The study, published today in Communications Biology, drives home that “understanding ancient virus evolution may be key to our understanding of [life’s] early developments,” says Simon Roux, a microbiologist at the Department of Energy’s Joint Genome Institute who was not involved in the work.
Giant viruses have amazed biologists since their discovery in 2003. They can be larger than some bacteria, their genomes are many times bigger than those of most viruses, and they have some characteristics of bacteria and other cellular forms of life. Biologists have found giant viruses in the deep sea and hiding in the genomes of red algae. They also inhabit hot springs—places Andreas Weber, a biochemist at Heinrich Heine University Düsseldorf, calls “time capsules that provide a window into early eukaryotic life.”
To learn more about how well-established giant viruses are in hot springs and what role they play there, Rutgers University genome scientist Debashish Bhattacharya and his colleagues harnessed new technologies for sequencing and analyzing DNA. They focused on Lemonade Creek, a very acidic hot spring creek in Yellowstone whose temperatures hover around 44°C. The creek’s floor is covered by a thick green mat that—despite its color—consists of Rhodophyta, or red algae. Researchers took samples from the mat, the adjacent soil, and the space between nearby rocks lying nearby. They sequenced all of the DNA in the samples.
From that harvest, postdoc Felipe Benites culled all known sequences from archaea, algae, and bacteria. That left him with DNA from about 3700 potential viruses; surprisingly, almost two-thirds of them were giant viruses. Using further computer analysis, Benite and his colleagues were able to piece together most of the genomes of about 25 different types of viruses. They think these reproduce by infecting the red algae.
Because hot springs come and go over geological time, the researchers assumed none of the giant viruses would be very old; they thought new viruses moved in from cooler environments and adapted to high temperatures every time a hot spring appeared somewhere. But their biomolecules told a different story. “The connections between the viruses and [their hosts] are ancient,” Bhattacharya says.
For one, viral proteins bore the hallmarks of a longtime hot spring dweller: They tended to have shorter loops and be more tightly packed than proteins adapted to milder conditions. Moreover, their DNA was “biased” to have the same three-base codes that other hot spring inhabitants have. And when the researchers reconstructed a viral family tree based on the newly sequenced viruses and other viral genes, they concluded that the hot spring viruses branched off very early in viral history. Their association with red algae likely dates back 1.5 billion years, the team reports.
“This work supports the concept that viruses are present wherever cellular life exists, that viruses have existed at least as long as cellular life,” says Mark Young, an environmental virologist emeritus at Montana State University who was not involved with the work.
They may also help solve an evolutionary puzzle. Many hot spring inhabitants borrowed genes from one another to cope with the heat and toxins such as arsenic, but exactly how more complex organisms such as algae did that is “elusive,” says Weber, who has studied how red algae swap genes for a decade. Viruses may have been the intermediaries, he and others think, readily taking on genes from bacteria and archaea and passing them on to the eukaryotes they infect. In that role, “the viruses likely play an important role in the long-term stability of the hot spring communities,” Weber says.
Bhattacharya suspects the viruses may have been important in another way: As they infected algal cells, they caused them to break apart, making their contents available for other cells to grow in an environment where nutrients were scarce.
The researchers made another surprising discovery: The viral communities on the algal mat, in the soil, and between the rocks were surprisingly different. “I would have thought that there would be more exchange between neighboring sites that are sometimes only a few centimeters apart,” Weber says. How and why these communities stay so isolated is another mystery, Young says—which “points out how little we really know about the diversity and role of viruses in microbial communities.”
