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

Nature Microbiology (2024)Cite this article

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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.

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Fig. 1: A pipeline for detecting host–virus pairs in the natural environment.
Fig. 2: Pairing between host cells and their actively infecting giant viruses.
Fig. 3: Single-cell metatranscriptome of co-occurring viral infections of diverse protist groups.
Fig. 4: Characterization of the predicted Leucocryptos virus genome and its suggested impact on the population dynamic of Katablepharidaceae.

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Data availability

Sequencing data have been deposited under NCBI Bioproject, accession no. PRJNA694552, Biosamples SAMN38317978–SAMN38317987. Additional data used in this paper, including UMI tables generated from 10x Cell Ranger, extended Blast result tables, assembled transcripts and other files that can be used to reproduce our results, are available at Dryad via https://doi.org/10.5061/dryad.s7h44j1c9 (ref. 76). Source data are provided with this paper. Public databases that were used in this manuscript include: the Giant Virus database https://faylward.github.io/GVDB; PR2 database https://pr2-database.org; metaPR2 database https://shiny.metapr2.org/metapr2; RefSeq v.207.

Code availability

All data management and analysis codes are open for review and reuse and archived online at GitHub via https://github.com/vardilab/host-virus-pairing (ref. 77).

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Acknowledgements

We thank Adva Shemi and Roi Avraham for their comments and suggestions for this manuscript. We thank Talia Shaler for helping to explain the technical aspects of 10x sequencing. We thank all AQUACOSM VIMS-Ehux project team members for conducting the mesocosm experiment. The present study was supported by the Simons Foundation grant (no. 735079), ‘Untangling the infection outcome of host–virus dynamics in algal blooms in the ocean’ awarded to A.V., the National Science Foundation award (no. 2141862) to F.O.A. and National Institutes of Health grant (no. 1R35GM147290-01) awarded to F.O.A.

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Author notes

  1. Gur Hevroni

    Present address: Google Geo, Tel Aviv, Israel

  2. Flora Vincent

    Present address: Developmental Biology Unit, European Molecular Biological Laboratory, Heidelberg, Germany

  3. These authors contributed equally: Amir Fromm, Gur Hevroni.

Authors and Affiliations

  1. Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel

    Amir Fromm, Gur Hevroni, Flora Vincent, Daniella Schatz & Assaf Vardi

  2. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    Carolina A. Martinez-Gutierrez & Frank O. Aylward

  3. Center for Emerging, Zoonotic, and Arthropod-Borne Pathogens, Virginia Tech, Blacksburg, VA, USA

    Frank O. Aylward

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Contributions

A.F., G.H., F.O.A. and A.V. designed and conceptualized the project and wrote the paper. A.F. and G.H. designed and wrote the scripts for data analysis. F.V. and D.S. collected the natural samples and prepared the single-cell transcriptomics libraries. F.O.A. and C.A.M.G. conducted phylogenetic analysis and viral homology search. A.F. conducted all other data analyses. All authors read and edited the manuscript.

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Correspondence to Frank O. Aylward or Assaf Vardi.

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Nature Microbiology thanks Anne-Kristin Kaster, Hiroyuki Ogata and J. Cesar Ignacio-Espinoza for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phylogenetic trees of giant virus marker genes assembled from the single-cell data.

Points denote transcripts assembled from single-cell transcriptomes. Numbers denote cells for which transcripts are present in both viral and host trees. a, 18 S rRNA (host). b, Major Capsid Protein (virus). c, DNA-Polymerase family B (virus).

Source data

Extended Data Fig. 2 Phylogenetic trees of functional genes present in the predicted Leucocryptos virus.

The different colors represent bacteria (red), eukaryotes (green), or giant viruses (purple). Arrows point at the location of the predicted Leucocryptos virus genes. a, Bax-1 apoptosis inhibitor. b, Metacaspase. c, heat-shock protein 90. d, heat-shock protein 70.

Extended Data Fig. 3 Cell abundance of calcified Emiliania huxleyi cells during bloom succession in the mesocosm experiment.

Calcified E. huxleyi cell count in bag no. 4 was measured by flow cytometry based on high side scatter and high chlorophyll signals.

Extended Data Fig. 4 Phylogenetic tree of Katablepharidaceae ASVs, 18 S rRNA sequences from PR2 database, and single-cell assembled Leucocryptos 18 S rRNA gene.

The different colors represent the different taxonomic groups analyzed. Filled dots denote ASV sequences, while empty dots denote PR2 sequences. The arrow points at the location of the single-cell assembled Leucocryptos 18S rRNA gene (in a triangle).

Supplementary information

Reporting Summary

Supplementary Table 1

All 972 infected cells before filtering with raw UMI counts. Blast results of assembled transcripts from the infected Katablepharidaceae subpopulation against different databases.

Source data

Source Data Fig. 2

Alternative names and colours assigned to taxa and raw UMI counts for host–virus pairs.

Source Data Fig. 3

Alternative names and colours assigned to taxa

Source Data Fig. 4

Genomic features, gene annotations and gene expression of the virus GVMAG-M-3300020187-27, for reproducing Fig. 4.

Source Data Extended Data Fig.1 and Table 1

Cell ID and barcode of cells present on both the viral and the host phylogenetic trees.

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Fromm, A., Hevroni, G., Vincent, F. et al. Single-cell RNA-seq of the rare virosphere reveals the native hosts of giant viruses in the marine environment. Nat Microbiol (2024). https://doi.org/10.1038/s41564-024-01669-y

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