Beetle poop may have helped shape millions of years of yeast evolution

University at Buffalo scientists have found evidence that different species of yeast have shared genes originally acquired from an ancient virus—and the guts and droppings of beetles may have helped make it happen.

Published in Molecular Biology and Evolution, the study shows that genetic material from that virus has evolved into a cluster of four related genes in yeasts in the genus Scheffersomyces. The study found that the cluster has moved between different species of these yeasts at least three times.

The yeasts, known for their promise in biofuel research, live on rotting wood and in the guts of beetles and other wood-eating insects, where they help their hosts digest wood. The researchers suspect that insects may have brought different yeast species together in their digestive tracts and excrement, creating opportunities for genetic exchange.

"It's an evolutionary whodunit, and wood-eating insects had the means and opportunity," says corresponding author Derek Taylor, Ph.D., professor of biological sciences in the UB College of Arts and Sciences.

The study makes several findings about the cluster, which the researchers have named STORM (Scheffersomyces Totivirus-like ORF Repeat Module). The cluster has persisted in yeast genomes for at least 15 million years, yet its genes have evolved at unexpectedly high rates: about seven times faster than their counterparts in related viruses.

"These genes have had an extraordinary evolutionary afterlife," says co-author Dominic Tringali, a master's student in Taylor's lab. "Long after the original virus disappeared, its genes continued to evolve, multiply and spread between yeast species."

A viral origin story

Taylor and collaborators first discovered these unusual viral genes in yeast in 2009 and proposed that genes like them might move between species.

"Now we have compelling evidence that an entire four-gene cluster has crossed species boundaries," Taylor says.

The ancient virus that infected the yeast is related to modern totiviruses, which are nonretroviral RNA viruses. Unlike retroviruses such as HIV, these viruses lack the machinery to convert their RNA into DNA and insert it into a host's genome on their own.

The researchers believe the viral RNA was somehow copied into DNA and incorporated into the yeast genome.

"To our knowledge, this is the first documented example of horizontal transfer of a cluster of duplicated genes derived from an ancient RNA virus," Taylor says.

Crossing species boundaries

The STORM genes' evolutionary histories didn't match those of the yeast species carrying them, suggesting the genes had moved between species rather than simply being inherited from common ancestors.

The researchers found evidence that the viral gene cluster crossed species boundaries through a process known as horizontal gene transfer—the movement of genetic material between organisms without ordinary reproduction.

At least one transfer appears to have happened through a transposon, or jumping gene. Transposons are segments of DNA that can move within genomes, and some can even move between species.

"Because STORM and a neighboring jumping gene show evidence of the same unusual evolutionary history, we suspect the transposon may have carried STORM between yeast species as extra cargo," Tringali says.

Wood-eating insects may have enabled the transposon to make the jump. Scheffersomyces yeasts often live as symbionts in their guts, where several species can coexist. Multiple species can also occur together in termite droppings and chewed wood that collect near rotting wood.

"In order to exchange genomic material, you have to be in the same place at the same time," Taylor says.

The jury is out on what the genes do

One of the study's most unusual findings is that the four genes, despite sharing a common viral origin, have followed different evolutionary paths.

Some have retained more of their ancestral virus-like protein structures, while others have changed extensively. This suggests that becoming part of the yeast genome freed the genes from at least some constraints imposed by their original viral roles. Yet natural selection appears to have preserved certain features of their sequences and protein structures, suggesting that these features still matter.

The genes have persisted for millions of years and remain together as a four-gene unit, even after moving between yeast species. All four are transcribed into RNA, and there is evidence that at least one produces a protein.

Together, these clues suggest that STORM may provide some benefit to yeast, but exactly what it does remains a mystery. Taylor suspects they may help yeast cope with stress.

"Totiviruses are kind of like a frenemy for yeast. Under some conditions, they help the host deal with physiological stress," he says. "So it might be useful for a yeast to keep a virus' benefits around without having to worry about controlling the virus."

The researchers hope to grow yeasts under different environmental stresses to see whether the STORM genes respond differently and potentially uncover what role the genes now play in their hosts.