Abstract

Our knowledge of the diversity and evolution of the virosphere will likely increase dramatically with the study of microbial eukaryotes, including the microalgae within which few RNA viruses have been documented. By combining total RNA sequencing with sequence and structural-based homology detection, we identified 18 novel RNA viruses in cultured samples from two major groups of microbial algae: the chlorophytes and the chlorarachniophytes. Most of the RNA viruses identified in the green algae class Ulvophyceae were related to the Tombusviridae and Amalgaviridae viral families commonly associated with land plants. This suggests that the evolutionary history of these viruses extends to divergence events between algae and land plants. Seven Ostreobium sp-associated viruses exhibited sequence similarity to the mitoviruses most commonly found in fungi, compatible with horizontal virus transfer between algae and fungi. We also document, for the first time, RNA viruses associated with chlorarachniophytes, including the first negative-sense (bunya-like) RNA virus in microalgae, as well as a distant homolog of the plant virus Virgaviridae, potentially signifying viral inheritance from the secondary chloroplast endosymbiosis that marked the origin of the chlorarachniophytes. More broadly, these data suggest that the scarcity of RNA viruses in algae results from limited investigation rather than their absence.

Highlights

  • Viruses are likely to infect every cellular organism and play fundamental roles in biosphere diversity, evolution, and ecology

  • We aimed to reveal more of the RNA virosphere in cultured samples of two clades of microalgae: (i) the green algae (Chlorophyta), that are part of the Archaeplastida eukaryotic supergroup, and (ii) the chlorarachniophytes, a lineage of Rhizaria that obtained a chloroplast through secondary endosymbiosis of a green alga [33]

  • Pictures illustrate some of the samples used in this study and corresponding clades are marked with “*”. (B) Pictures of algae cultures used in this study. (C) The current extent of the microalgae virosphere

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Summary

Introduction

Viruses are likely to infect every cellular organism and play fundamental roles in biosphere diversity, evolution, and ecology. Those studies of the global virosphere performed to date have revealed marked heterogeneities in virus composition. While RNA viruses are commonplace in eukaryotes, they are less often found in bacteria and are yet to be conclusively identified in archaea. Rather, both the bacteria and archaea are dominated by DNA viruses [1,2]. Whether such highly skewed virus distributions reflect fundamental biological, cellular or ecological factors of the hosts in question, or because RNA viruses in bacteria and archaea are often so divergent in sequence that they are difficult to detect using primary sequence comparisons alone.

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