Over two decades of research on the marine RNA virosphere

Abstract

RNA viruses (realm: Riboviria), including RNA phages and eukaryote‐infecting RNA viruses, are essential components of marine ecosystems. A large number of marine RNA viruses have been discovered in the last two decades because of the rapid development of next‐generation sequencing (NGS) technology. Indeed, the combination of NGS and state‐of‐the‐art meta‐omics methods (viromics, the study of all viruses in a specific environment) has led to a fundamental understanding of the taxonomy and genetic diversity of RNA viruses in the sea, suggesting the complex ecological roles played by RNA viruses in this complex ecosystem. Furthermore, comparisons of viromes in the context of highly variable marine niches reveal the biogeographic patterns and ecological impact of marine RNA viruses, whose role in global ecology is becoming increasingly clearer. In this review, we summarize the characteristics of the global marine RNA virosphere and outline the taxonomic hierarchy of RNA viruses with a specific focus on their ancient evolutionary history. We also review the development of methodology and the major progress resulting from its applications in RNA viromics. The aim of this review is not only to provide an in‐depth understanding of multifaceted aspects of marine RNA viruses, but to offer future perspectives on developing a better methodology for discovery, and exploring the evolutionary origin and major ecological significance of marine RNA virosphere.

Novel RNA viruses from the Atlantic Ocean: Ecogenomics, biogeography, and total virioplankton mass contribution from surface to the deep ocean

“…RdRP is likely on of the best hallmark genes for RNA viruses (Liao et al, 2022). Hence, to study the composition of the viral population of each sample (Figure 3A), we observed the distribution of different RdRP models on the samples (Figure 3C) complemented it with a principal component analysis (PCA) (Figure 3B).…”

“…In contrast, RNA viruses tend to infect protists and other eukaryotic organisms, which makes their hosts fairly less abundant (Lang et al, 2009). Furthermore, the study of RNA viruses presents both culture‐dependent and ‐independent methodological limitations due to the difficulty of isolating viruses and hosts in addition to the relatively smaller genome size and higher taxonomic diversity that complicate the metagenomic surveys (Liao et al, 2022). These reasons explain why the study of RNA viruses has remained relatively unexplored by the scientific community until recent years (Callanan et al, 2020; Dominguez‐Huerta et al, 2023; Zayed et al, 2022).…”

“…Moreover, the significance of RNA viruses in biogeochemical cycles has been shown to be greater than previously believed, with specific RNA viral species having a direct impact on ocean carbon export (Dominguez‐Huerta et al, 2022). But all these previous studies have been conducted in specific environments with limited areas of focus, primarily in coastal waters from temperate regions and the Antarctic ocean, or using metaviromes or metatranscriptomes available from the Tara dataset (Culley et al, 2006; Culley et al, 2014; Culley & Steward, 2007; Liao et al, 2022; Miranda et al, 2016).…”

The RNA virosphere: How big and diverse is it?

“…A decade later, sequencing technologies had advanced sufficiently to enable the exploration of diverse environments, often via mining RdRp sequences in RNA‐seq data derived from (i) biotic samples (including holobiont, unicellular, and multicellular organisms), such as invertebrates (Li et al, 2015; Shi et al, 2016; Vieira et al, 2022b; Wu et al, 2020), vertebrates (Shi et al, 2018), plants (Roossinck, 2012; Vieira et al, 2022a), protists (Cai et al, 2012; Charon et al, 2022, 2020, 2021; Lachnit et al, 2015; Nagasaki et al, 2004; Sasai et al, 2018; Shirai et al, 2008; Tai et al, 2003; Tomaru et al 2004, 2009, 2012), and fungi (Deakin et al, 2017; Marzano et al, 2016) and (ii) environmental samples, such as faeces (Krishnamurthy et al, 2016), sediments (Callanan et al, 2020), soils (Hillary et al, 2022; Starr et al, 2019; Wu et al, 2021), rivers (French et al, 2022), and seawater from specific sites (Culley et al, 2003, 2006, 2014; Djikeng et al, 2009; Steward et al, 2013; Urayama et al, 2018; Vlok et al, 2019; Wolf et al, 2020) and from geographic locations representing the entire global oceans (Dominguez‐Huerta et al, 2022; Zayed et al, 2022). The environments most explored for RNA viruses during these two decades are aquatic (e.g., marine, sewage, and riverine), providing us with the first insights into their ecology, evolution of their viral inhabitants, and methodological challenges associated with characterizing specific natural ecosystems (Culley, 2018; Liao et al, 2022). In all, although RNA virus taxonomy is under constant development, 20 years of metagenomic and metatranscriptomic surveys have moved the needle from a few thousand formally‐defined RNA virus species to more than 100,000 species‐rank taxa (Neri et al, 2022) that have yet to be officially recognized by the International Committee on Taxonomy of Viruses (ICTV) and a growing number of orthornaviran phyla (Neri et al, 2022; Zayed et al, 2022) (Figu...…”

Development of a multiplex qRT-PCR assay for the detection of porcine epidemic diarrhea virus, porcine transmissible gastroenteritis virus and porcine Deltacoronavirus

“…Coronaviruses belonging to the family Coronaviridae, the order Nidovirales, are single-stranded, positive-sense RNA viruses with the largest genome among known RNA viruses (1)(2)(3). Within swine enteric viruses, coronaviruses are the most devastating pathogens responsible for acute diarrhea, vomiting, dehydration, and high mortality in neonatal and suckling piglets (4)(5)(6).…”