Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome

Abstract

Whereas DNA viruses are known to be abundant, diverse, and commonly key ecosystem players, RNA viruses are insufficiently studied outside disease settings. In this study, we analyzed ≈28 terabases of Global Ocean RNA sequences to expand Earth’s RNA virus catalogs and their taxonomy, investigate their evolutionary origins, and assess their marine biogeography from pole to pole. Using new approaches to optimize discovery and classification, we identified RNA viruses that necessitate substantive revisions of taxonomy (doubling phyla and adding >50% new classes) and evolutionary understanding. “Species”-rank abundance determination revealed that viruses of the new phyla “ Taraviricota ,” a missing link in early RNA virus evolution, and “ Arctiviricota ” are widespread and dominant in the oceans. These efforts provide foundational knowledge critical to integrating RNA viruses into ecological and epidemiological models.

Diversity and ecological footprint of Global Ocean RNA viruses

“…However, none of these global studies included RNA viruses. Hence, we used our previously generated RNA vOTUs ( 19 ), preclustered at 90% average nucleotide identity across 80% of the shorter sequence length and 1-kb minimum contig length (materials and methods), and their relative abundances, estimated by means of metatranscriptomic read mapping (materials and methods), to investigate marine RNA virus ecology globally.…”

“…Despite literature increasingly presenting RNA viruses as a likely major force behind biogeochemistry ( 6 , 14 , 15 ), empirical data are challenging to obtain. Recent sequencing surveys, including from the oceans, have identified thousands of previously unknown RNA viruses that constitute genus- or subfamily-rank taxa ( 16 – 18 ) as well as phylum-rank taxa ( 19 ). However, research on the ecology of RNA viruses has been limited to small spatial scales among pelagic waters and/or viruses associated with larger plankton of a few species (table S1).…”

“…1A, fig. S1, table S2 for sample metadata, and materials and methods) to identify and quantify RNA viruses ( 19 ). This effort led to the identification of 44,779 RNA virus contigs that were dereplicated to 5504 “species”-level virus operational taxonomic units (vOTUs), for which we established taxonomy, evolutionary origins, and biogeography.…”

Diverse RNA viruses associated with diatom, eustigmatophyte, dinoflagellate and rhodophyte microalgae cultures

“…By avoiding cultivation limitations and paving the way for the exploration of very diverse environments (soil, water, etc. ), the metagenomic era has multiplied the number of RNA viruses described by many thousands [10][11][12][13] . This is particularly evident in the field of "phycovirology" (the study of algal viruses), for which recent studies investigating RNA viruses using metagenomic approaches have revealed a high diversity and prevalence of RNA viruses in several microalgae lineages 11,[14][15][16][17][18][19][20][21] .…”

Integrated analysis of intestinal microbiota and metabolomic reveals that decapod iridescent virus 1 (DIV1) infection induces secondary bacterial infection and metabolic reprogramming in Marsupenaeus japonicus

“…Viruses are an important part of marine ecosystems. With the development of genetic technology, more and more new marine RNA and DNA viruses have been discovered (Gregory et al, 2019; Zayed et al, 2022). Despite their tiny size, viruses play a large role in marine ecosystems and food webs.…”