Phaeoviruses are latent double-stranded DNA viruses that insert their genomes into those of their brown algal (Phaeophyceae) hosts. So far these viruses are known only from members of the Ectocarpales, which are small and short-lived macroalgae. Here we report molecular and morphological evidence for a new Phaeovirus cluster, referred to as sub-group C, infecting kelps (Laminariales) of the genera Laminaria and Saccharina, which are ecologically and commercially important seaweeds. Epifluorescence and TEM observations indicate that the Laminaria digitata Virus (LdigV), the type species of sub-group C, targets the host nucleus for its genome replication, followed by gradual degradation of the chloroplast and assembly of virions in the cytoplasm of both vegetative and reproductive cells. This study is the first to describe phaeoviruses in kelp. In the field, these viruses infected two thirds of their host populations; however, their biological impact remains unknown.

Two sister orders of the brown macroalgae (class Phaeophyceae), the morphologically complex Laminariales (commonly referred to as kelp) and the morphologically simple Ectocarpales are natural hosts for the dsDNA phaeoviruses (family Phycodnaviridae) that persist as proviruses in the genomes of their hosts. We have previously shown that the major capsid protein (MCP) and DNA polymerase concatenated gene phylogeny splits phaeoviruses into two subgroups, A and B (both infecting Ectocarpales), while MCP-based phylogeny suggests that the kelp phaeoviruses form a distinct third subgroup C. Here we used MCP to better understand the host range of phaeoviruses by screening a further 96 and 909 samples representing 11 and 3 species of kelp and Ectocarpales, respectively. Sporophyte kelp samples were collected from their various natural coastal habitats spanning five continents: Africa, Asia, Australia, Europe, and South America. Our phylogenetic analyses showed that while most of the kelp phaeoviruses, including one from Macrocystis pyrifera, belonged to the previously designated subgroup C, new lineages of Phaeovirus in 3 kelp species, Ecklonia maxima, Ecklonia radiata, Undaria pinnatifida, grouped instead with subgroup A. In addition, we observed a prevalence of 26% and 63% in kelp and Ectocarpales, respectively. Although not common, multiple phaeoviral infections per individual were observed, with the Ectocarpales having both intra- and inter-subgroup phaeoviral infections. Only intra-subgroup phaeoviral infections were observed in kelp. Furthermore, prevalence of phaeoviral infections within the Ectocarpales is also linked to their exposure to waves. We conclude that phaeoviral infection is a widely occurring phenomenon in both lineages, and that phaeoviruses have diversified with their hosts at least since the divergence of the Laminariales and Ectocarpales.

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Photosynthesis originated from endosymbiosis of cyanobacterial‐like organisms, which ultimately became chloroplasts. It is an ancient process that has evolved to produce a variety of types of photosynthetic eukaryotic organisms that we find today, that is, terrestrial plants and aquatic algae. Similarly, viruses are considered ancient with growing evidence for the theory that viruses arose before the last universal cellular ancestor. Despite both photosynthetic and virus life forms having evolved side by side since time immemorial, plants and eukaryotic algae have very different viruses that infect them. Very little similarities are shared in both the types and nature of the infection. In fact, viruses of photosynthetic eukaryotic multicellular organisms exemplify how different algae are from plants. Key Concepts Photosynthetic organisms appeared 3.2–3.5 billion years ago. The most abundant and diverse viruses have dsDNA genomes. NCLDVs are estimated to have evolved 2–2.7 billion years ago, close to the origin of eukaryotes. The known host range of NCLDVs includes multiple eukaryotic kingdoms, which is the broadest of any dsDNA virus group, which usually infect a single kingdom. The family Phycodnaviridae (‘phyco’=algae, ‘dna’=DNA, ‘viridae’=virus family) are NCLDVs that infect algae. Most plant viruses (66.7%) have ssRNA genomes. Plant viruses use long‐distance transport as a key mechanism for transmission. This would be possible in some macroalgae which have vascular tissue (sieve tubes), such as kelps, but these sieve tubes are less extensive than the xylem and phloem of plants. The NCLDVs are a major algal virus group which may be absent in plants, which are instead predominately infected by ssRNA viruses. Eukaryotic multicellular macroalgae or seaweed are predominantly infected by dsDNA viruses.

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