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Single-cell RNA-seq of the rare virosphere reveals the native hosts of giant viruses in the marine environment.

ABSTRACT: Giant viruses (phylum Nucleocytoviricota) are globally distributed in aquatic ecosystems. They play fundamental roles as evolutionary drivers of eukaryotic plankton and regulators of global biogeochemical cycles. However, we lack knowledge about their native hosts, hindering our understanding of their life cycle and ecological importance. In the present study, we applied a single-cell RNA sequencing (scRNA-seq) approach to samples collected during an induced algal bloom, which enabled pairing active giant viruses with their native protist hosts. We detected hundreds of single cells from multiple host lineages infected by diverse giant viruses. These host cells included members of the algal groups Chrysophycae and Prymnesiophycae, as well as heterotrophic flagellates in the class Katablepharidaceae. Katablepharids were infected with a rare Imitervirales-07 giant virus lineage expressing a large repertoire of cell-fate regulation genes. Analysis of the temporal dynamics of these host-virus interactions revealed an important role for the Imitervirales-07 in controlling the population size of the host Katablepharid population. Our results demonstrate that scRNA-seq can be used to identify previously undescribed host-virus interactions and study their ecological importance and impact.

SUBMITTER: Fromm A

PROVIDER: S-EPMC11265207 | biostudies-literature | 2024 Jun

REPOSITORIES: biostudies-literature

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Single-cell RNA-seq of the rare virosphere reveals the native hosts of giant viruses in the marine environment.

Fromm Amir A Hevroni Gur G Vincent Flora F Schatz Daniella D Martinez-Gutierrez Carolina A CA Aylward Frank O FO Vardi Assaf A

Nature microbiology 20240411 6

Giant viruses (phylum Nucleocytoviricota) are globally distributed in aquatic ecosystems. They play fundamental roles as evolutionary drivers of eukaryotic plankton and regulators of global biogeochemical cycles. However, we lack knowledge about their native hosts, hindering our understanding of their life cycle and ecological importance. In the present study, we applied a single-cell RNA sequencing (scRNA-seq) approach to samples collected during an induced algal bloom, which enabled pairing ac ...[more]

PMID: 38605173

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Project description:Arctic permafrost is thawing due to global warming, with unknown consequences on the microbial inhabitants or associated viruses. DNA viruses have previously been shown to be abundant and active in thawing permafrost, but little is known about RNA viruses in these systems. To address this knowledge gap, we assessed the composition of RNA viruses in thawed permafrost samples that were incubated for 97 days at 4°C to simulate thaw conditions. A diverse RNA viral community was assembled from metatranscriptome data including double-stranded RNA viruses, dominated by Reoviridae and Hypoviridae, and negative and positive single-stranded RNA viruses, with relatively high representations of Rhabdoviridae and Leviviridae, respectively. Sequences corresponding to potential plant and human pathogens were also detected. The detected RNA viruses primarily targeted dominant eukaryotic taxa in the samples (e.g., fungi, Metazoa and Viridiplantae) and the viral community structures were significantly associated with predicted host populations. These results indicate that RNA viruses are linked to eukaryotic host dynamics. Several of the RNA viral sequences contained auxiliary metabolic genes encoding proteins involved in carbon utilization (e.g., polygalacturosase), implying their potential roles in carbon cycling in thawed permafrost. IMPORTANCE Permafrost is thawing at a rapid pace in the Arctic with largely unknown consequences on ecological processes that are fundamental to Arctic ecosystems. This is the first study to determine the composition of RNA viruses in thawed permafrost. Other recent studies have characterized DNA viruses in thawing permafrost, but the majority of DNA viruses are bacteriophages that target bacterial hosts. By contrast RNA viruses primarily target eukaryotic hosts and thus represent potential pathogenic threats to humans, animals, and plants. Here, we find that RNA viruses in permafrost are novel and distinct from those in other habitats studied to date. The COVID-19 pandemic has heightened awareness of the importance of potential environmental reservoirs of emerging RNA viral pathogens. We demonstrate that some potential pathogens were detected after an experimental thawing regime. These results are important for understanding critical viral-host interactions and provide a better understanding of the ecological roles that RNA viruses play as permafrost thaws.

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Single-cell RNA-seq of the rare virosphere reveals the native hosts of giant viruses in the marine environment.

Publications

Single-cell RNA-seq of the rare virosphere reveals the native hosts of giant viruses in the marine environment.

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