Viroid-like “obelisk” agents are widespread in the ocean and exceed the abundance of RNA viruses in the prokaryotic fraction

“Obelisks” are recently discovered RNA viroid-like elements present in diverse environments with no phylogenetic similarity to any known biological agent. Obelisks were first identified in the human gut and in a commensal bacterium acting as a replicative host. They have a circular ∼1 kb RNA genome, rod-like secondary structures, and the encoding of a protein superfamily called “Oblins”. We performed a large-scale search of Obelisks in the ocean using the Pebblescout program and the transcriptomic Sequence Archive Read databases, revealing the biogeography and abundance of these viroid-like RNA elements. We detected 45 Obelisk genomes resulting in 35 marine clusters at the species level. These Obelisks were detected in the prokaryotic fraction and to a lesser extent in the eukaryotic fraction, and distributed across all the oceans from surface to mesopelagic including the Arctic, and even in the coldest seawater of Earth beneath the Antarctic Ross Ice Shelf. The Obelisk hallmark protein Oblin-1 confirmed by 3D models was found in various marine samples. Some of the detected marine Obelisks harbour hammerhead self-cleaving ribozymes in both polarities. In the prokaryotic, but not the eukaryotic, fraction of the Tara Ocean dataset, relative abundance of Obelisks calculated by transcriptomic fragment recruitment indicated that they are abundant in marine samples, reaching or even exceeding the relative abundance of the previously discovered uncultured RNA viruses. In conclusion, Obelisks are abundant and widespread viroid-like elements that should be included in ocean biogeochemical models.