Freshwater macrophytes harbor viruses representing all five major phyla of the RNA viral kingdom Orthornavirae

Abstract

Research on aquatic plant viruses is lagging behind that of their terrestrial counterparts. To address this knowledge gap, here we identified viruses associated with freshwater macrophytes, a taxonomically diverse group of aquatic phototrophs that are visible with the naked eye. We surveyed pooled macrophyte samples collected at four spring sites in Florida, USA through next generation sequencing of RNA extracted from purified viral particles. Sequencing efforts resulted in the detection of 156 freshwater macrophyte associated (FMA) viral contigs, 37 of which approximate complete genomes or segments. FMA viral contigs represent putative members from all five major phyla of the RNA viral kingdom Orthornavirae. Similar to viral types found in land plants, viral sequences identified in macrophytes were dominated by positive-sense RNA viruses. Over half of the FMA viral contigs were most similar to viruses reported from diverse hosts in aquatic environments, including phototrophs, invertebrates, and fungi. The detection of FMA viruses from orders dominated by plant viruses, namely Patatavirales and Tymovirales, indicate that members of these orders may thrive in aquatic hosts. PCR assays confirmed the presence of putative FMA plant viruses in asymptomatic vascular plants, indicating that viruses with persistent lifestyles are widespread in macrophytes. The detection of potato virus Y and oat blue dwarf virus in submerged macrophytes suggests that terrestrial plant viruses infect underwater plants and highlights a potential terrestrial-freshwater plant virus continuum. Defining the virome of unexplored macrophytes will improve our understanding of virus evolution in terrestrial and aquatic primary producers and reveal the potential ecological impacts of viral infection in macrophytes.

ICTV Virus Taxonomy Profile: Yueviridae 2023

“…The yuevirid genome comprises two segments of linear negative-sense RNA with a total length of 7.8–8.2 kb (large (L) segment, 6.6–6.9 kb; small (S) segment, 1.2–1.3 kb) [1–5] (, ). The L segment ORF ( L ) encodes an RNA-directed RNA polymerase (RdRP) with a GDP : polyribonucleotidyltransferase (PRNTase) domain that is related to that of viruses in the order Mononegavirales , suggesting a similar capping mechanism.…”

“…The family Yueviridae includes at least one genus and two species for the viruses Běihǎi sesarmid crab virus 3 and Shāhé yuevirus-like virus 1, found in unspecified sesarmid crabs (Crustacea: Decapoda) and freshwater isopods (Crustacea: Isopoda), respectively, in China [1] (). Unclassified yuevirids have been associated with diverse crustaceans and insects [6], stramenopiles [7–9], tracheophytes [3], and unspecified macrophytes [5]. Thus, the diversity of yuevirids is likely vastly underestimated [2, 4].…”

“…2). Unclassified yuevirids have been associated with diverse crustaceans and insects [6], stramenopiles [7][8][9], tracheophytes [3], and unspecified macrophytes [5]. Thus, the diversity of yuevirids is likely vastly underestimated [2,4].…”

Identification of RNA Virus–Derived RdRp Sequences in Publicly Available Transcriptomic Data Sets

“…The ∼5,500 RNA virus (kingdom Orthornavirae) species currently represented in GenBank constitute just a tiny fraction of the estimated millions of RNA virus species on Earth ( Geoghegan and Holmes 2017 ; Kuhn et al 2019 ; Dance 2021 ; Harvey and Holmes 2022 ). Recent high-throughput RNA sequencing (RNA-Seq) studies—performed with the express purpose of identifying RNA viruses—have revealed vast numbers of novel RNA viruses, and many new family-level virus clades in diverse eukaryotic host organisms ( Cook et al 2013 ; Li et al 2015 ; Shi et al 2016 , 2018 ; Olendraite et al 2017 ; Charon et al 2020 ; Chiapello et al 2020 ; Sutela et al 2020 ; Wolf et al 2020 ; Batson et al 2021 ; Chen et al 2022 ; Forgia, Chiapello, et al 2022 ; Kinsella et al 2022 ; Rosario et al 2022 ; reviewed in Dolja and Koonin 2018 ; Greninger 2018 ; Obbard 2018 ; Zhang et al 2019 ; Cobbin et al 2021 ; Harvey and Holmes 2022 ). However, a much larger number of RNA-Seq studies are performed for projects that are unrelated to virus discovery, but instead aim to study the transcriptomes of the targeted cellular organisms.…”

Identification of RNA virus-derived RdRp sequences in publicly available transcriptomic datasets

“…The ∼5,500 RNA virus (kingdom Orthornavirae ) species currently represented in GenBank constitute just a tiny fraction of the estimated millions of RNA virus species on Earth (Geoghegan & Holmes, 2017; Kuhn et al, 2019; Dance, 2021; Harvey & Holmes, 2022). Recent high-throughput RNA sequencing (RNA-Seq) studies – performed with the express purpose of identifying RNA viruses – have revealed vast numbers of novel RNA viruses, and many new family-level virus clades in diverse eukaryotic host organisms (Cook et al, 2013; Li et al, 2015; Shi et al, 2016, 2018; Olendraite et al, 2017; Charon et al, 2020; Chiapello et al, 2020; Sutela et al, 2020; Wolf et al, 2020; Batson et al, 2021; Chen et al, 2022; Forgia et al, 2022a; Kinsella et al, 2022; Rosario et al, 2022; reviewed in Dolja & Koonin, 2018; Greninger, 2018; Obbard, 2018; Zhang et al, 2019; Cobbin et al, 2021; Harvey & Holmes, 2022). However, a much larger number of RNA-Seq studies are performed for projects that are unrelated to virus discovery, but instead aim to study the transcriptomes of the targeted cellular organisms.…”