Nearly complete set of translation-related genes lends support to hypothesis that giant viruses evolved from smaller viruses

An international team of researchers, including NCBI’s Eugene Koonin and Natalya Yutin, has discovered a novel group of giant viruses (dubbed “Klosneuviruses”) with a more complete set of translation machinery genes than any virus that has been described to date. “This discovery significantly expands our understanding of viral evolution,” said Koonin. “These are the most ‘cell-like’ viruses ever identified. However, the computational analysis of the virus genomes shows that these viruses have not evolved from cells by reductive evolution but rather have evolved from smaller viruses, gradually acquiring genes from their hosts at different stages of their evolution.”

The research was published in the journal Science on April 6, 2017. In addition to biologists from NCBI, the authors include collaborators from the U.S. Department of Energy Joint Genome Institute (DOE JGI), the University of Vienna, and CalTech.

JGI researchers Frederik Schulz and Tanja Woyke unearthed Klosneuvirus while analyzing microcolony sequence data from a wastewater treatment plant sample in Klosterneuburg, Austria. “We expected nitrifier genome sequences in the microcolony sequence data,” Woyke said. “Finding a giant virus genome took the project into a completely new and unexpected, yet very exciting, direction.” When Schulz noticed that several of the metagenomes were viral in origin, he and Woyke conducted analyses to determine their source. They found that the Klosneuvirus group came from a novel viral lineage affiliated with Mimiviruses, the first giant viruses discovered. A handful of other giant virus groups have been found since the discovery of Mimiviruses in 2003.

Giant viruses are characterized by disproportionately large genomes and virions that house viruses’ genetic material. They can encode several genes potentially involved in protein biosynthesis, a unique feature that has led to diverging hypotheses about their origin.Two evolutionary hypotheses have emerged. One posits that giant viruses evolved from an ancient cell, perhaps one from an extinct fourth domain of cellular life. Another — a scenario championed by Koonin — presents the idea that giant viruses descended from smaller viruses. The discovery of Klosneuvirus, Woyke said, supports the latter hypothesis. In this scenario, a smaller virus infected different eukaryote hosts and picked up genes from independent sources over long periods of time through piecemeal acquisition of translational machinery components.

“At first glance, the suite of “cellular” genes in Klosneuvirus seemed to have a common origin, but when we analyzed them in detail, we saw they came from different hosts,” Koonin said. “We could infer from the evolutionary trees we built that they have been acquired by the viruses piecemeal, at different stages in their evolution.” The Klosneuvirus genes contained aminoacyl-tRNA (transfer ribonucleic acid) enzymes with specificity for 19 out of 20 amino acids, along with more than 20 tRNAs and an array of translation factors and tRNA modifying enzymes—an unprecedented finding among any viruses, including the previously known giant viruses.

Schulz noted that while the metagenomic discovery of Klosneuviruses helped answer important evolutionary questions, the actual biological function of the translation system genes remains elusive—at least until these viruses are grown in the laboratory together with their hosts.

And Koonin believes there are more giant viruses waiting to be discovered in metagenomic data. “I’m quite confident that the current record of the genome size of giant viruses will be broken,” he said. “We are going to see the real Goliaths of the giant virus world.”

— Many thanks to JGI for their assistance in preparing this news feature.