Viroids: “living fossils” of primordial RNAs?

The discovery of the viroid in 1971, which initiated the third major expansion of the biosphere towards smaller living entities—after discovery of the “subvisual” microorganisms in 1675 and that of the “submicroscopic” viruses in 1892—has been officially endorsed by the International Committee on Virus Taxonomy as a new order called subviral agents. In 1989, I proposed that, based on their respective molecular properties, viroids are more plausible “living fossils” of the hypothetical RNA World (widely assumed to have existed prior to the evolution of DNA or proteins) than are intron-derived RNAs, which were, at that time, suggested as putative survivors. There were few citations of my proposal—and virtually none of viroids—beyond plant virology unil 1994, when Cheles-Flores critically examined the hypothesis and pointed out a serious difficulty, as well as a process by which this difficulty could be overcome. In 2013, when investigations by Koonin and Dolja revealed that of extant RNAs, viroids “strikingly” display some of the molecular properties posited for the earliest evolving, selfish RNAs (primordial RNAs), but, because extant organisms, aside from higher plants, appear not to harbor viroids, they cannot be regarded as primordial fossils, but appear to have evolved post LUCA (the Last Universal Common Ancestor). Here, I review whether some evidence nevertheless is compatible with the original postulate of the 1989 hypothesis. My analysis reveals no unequivocal evidence for an ancient origin of viroids, but suggests, alternatively, that viroids may have evolved de novo more recently, probably by novel processes similar to those suggested by each reviewer. These results are important, because they help illuminate a little understood period of abiogenesis—after the abiotic synthesis of life’s chemical building blocks, which is, in principle, understood, and before the evolution of DNA and proteins in the late RNA World.