In an article published in
Nature Microbiology, scientists reveal the existence of numerous new lineages of mirusviruses, giant viruses that swarm in the oceans.
While most giant viruses known to date replicate their DNA in the cytoplasm of the infected cell, they show that many mirusviruses have a lifestyle centered on replicating their DNA in the nucleus. This work reveals not only a major ecological niche for DNA viruses in plankton but also a uniquely unique evolutionary history.
Mirusviruses are DNA viruses with complex genomes, widely distributed in the oceans, seas, rivers, and lakes of the globe where they infect unicellular eukaryotes. Their discovery, initiated thanks to the
Tara Oceans expedition, already allowed in 2023 for the description of a first major group, the order
Demutovirales, and for a better understanding of the evolutionary history of the herpes virus. It also revealed the existence of a second genus of giant viruses associated with plankton, two decades after the discovery of a first genus: the nucleocytoviruses.
Mirusviruses form viral particles very different from those of nucleocytoviruses. These two lineages therefore cannot be grouped under the same taxonomic umbrella. However, the mirusviruses described in the first study shared a major trait with established giant viruses: the presence of essential functions including polymerases, which are enzymes that allow viral DNA replication and transcription directly in the cytoplasm of their hosts. Two lineages of giant viruses thus seemed to coexist, each with a distinct particle type, but both centered on cytoplasmic replication.
The new study completely overturns this model.
A second phylum of giant viruses, rich with unsuspected diversity
In an article published in the journal
Nature Microbiology, scientists have discovered numerous additional lineages of mirusviruses through the reconstruction and analysis of over 1200 environmental genomes.
Phylogenetic approaches allow them to propose a first expanded classification: mirusviruses would constitute a second phylum of giant viruses (after nucleocytoviruses) comprising two additional major orders (
Okeanovirales and
Styxvirales), a minor order (
Soporavirales), as well as 13 more enigmatic orders that seem to have a surprising evolutionary history due to their diversity but for which few viruses have been characterized to date.
Mirusviruses, centered on the nucleus and no longer on the host's cytoplasm
At the heart of the study are unexpected genetic characteristics, revealing a radically different lifestyle for most of the newly described mirusviruses.
Unlike mirusviruses of
Demutovirales (and most known giant viruses), most of the newly identified mirusviruses possess no polymerases, even though their genomes can reach half a million nucleotides. They therefore strongly depend on the host cell's replication and transcription enzymes, activities that occur exclusively in the nucleus.
Another surprise: their genes are scattered with spliceosomal introns, DNA segments that do not belong to the coding parts of genes. For the genes to produce functional RNA, these introns must be removed by the spliceosome, a cellular machinery that assembles coding sequences into a mature RNA. This step occurs exclusively in the nucleus, confirming a nuclear replication mode.
The researchers also discovered that these introns contain thousands of endonuclease genes, a combination never observed before, even in eukaryotes. Endonucleases are enzymes capable of cutting DNA inside a sequence (as opposed to exonucleases, which cut at the ends). In these mirusviruses, their presence in the introns suggests particularly active mechanisms of genetic mobility and genome remodeling, reinforcing the idea of a very dynamic evolutionary history of their intron richness.
Major questions still open
This study thus reveals that the nucleus of unicellular eukaryotes, key organisms of plankton that play a considerable ecological and evolutionary role, particularly in the context of global warming, is a niche for the replication of many DNA viruses with complex genomes. These mirusviruses therefore change our understanding of how plankton functions in general, and cell-virus interactions in particular.
Many questions remain:
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How did these viruses evolve towards two distinct lifestyles? One centered on the cytoplasm (
Demutovirales), the other on the nucleus (
Okeanovirales and
Styxvirales).
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Who are their main hosts? And how do they influence the physiology of unicellular eukaryotes on a large scale?
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Are nucleus + cytoplasm co-infections frequent? Can a cell be infected simultaneously by a cytoplasmic giant virus and a nuclear mirusvirus? Does this promote gene exchanges between viruses, notably with nucleocytoviruses?
Several international teams are already working on these questions, and the coming years should shed more light on the role and evolution of these astonishing giant viruses.