The genomic and phylogenetic analysis of Marseillevirus cajuinensis raises questions about the evolution of Marseilleviridae lineages and their taxonomical organization.

Marseilleviruses (MsV) are a group of viruses that compose the Marseilleviridae family within the Nucleocytoviricota phylum. They have been found in different samples, mainly in freshwater. MsV are classically organized into five phylogenetic lineages (A/B/C/D/E), but the current taxonomy does not fully represent all the diversity of the MsV lineages. Here, we describe a novel strain isolated from a Brazilian saltwater sample named Marseillevirus cajuinensis. Based on genomics and phylogenetic analyses, M. cajuinensis exhibits a 380,653-bp genome that encodes 515 open reading frames. Additionally, M. cajuinensis encodes a transfer RNA, a feature that is rarely described for Marseilleviridae. Phylogeny suggests that M. cajuinensis forms a divergent branch within the MsV lineage A. Furthermore, our analysis suggests that the common ancestor for the five classical lineages of MsV diversified into three major groups. The organization of MsV into three main groups is reinforced by a comprehensive analysis of clusters of orthologous groups, sequence identities, and evolutionary distances considering several MsV isolates. Taken together, our results highlight the importance of discovering new viruses to expand the knowledge about known viruses that belong to the same lineages or families. This work proposes a new perspective on the Marseilleviridae lineages organization that could be helpful to a future update in the taxonomy of the Marseilleviridae family. IMPORTANCE: Marseilleviridae is a family of viruses whose members were mostly isolated from freshwater samples. In this work, we describe the first Marseillevirus isolated from saltwater samples, which we called Marseillevirus cajuinensis. Most of M. cajuinensis genomic features are comparable to other Marseilleviridae members, such as its high number of unknown proteins. On the other hand, M. cajuinensis encodes a transfer RNA, which is a gene category involved in protein translation that is rarely described in this viral family. Additionally, our phylogenetic analyses suggested the existence of, at least, three major Marseilleviridae groups. These observations provide a new perspective on Marseilleviridae lineages organization, which will be valuable in future updates to the taxonomy of the family since the current official classification does not capture all the Marseilleviridae known diversity.

Giant Viruses as a Source of Novel Enzymes for Biotechnological Application.

The global demand for industrial enzymes has been increasing in recent years, and the search for new sources of these biological products is intense, especially in microorganisms. Most known viruses have limited genetic machinery and, thus, have been overlooked by the enzyme industry for years. However, a peculiar group of viruses breaks this paradigm. Giant viruses of the phylum Nucleocytoviricota infect protists (i.e., algae and amoebae) and have complex genomes, reaching up to 2.7 Mb in length and encoding hundreds of genes. Different giant viruses have robust metabolic machinery, especially those in the Phycodnaviridae and Mimiviridae families. In this review, we present some peculiarities of giant viruses that infect protists and discuss why they should be seen as an outstanding source of new enzymes. We revisited the genomes of representatives of different groups of giant viruses and put together information about their enzymatic machinery, highlighting several genes to be explored in biotechnology involved in carbohydrate metabolism, DNA replication, and RNA processing, among others. Finally, we present additional evidence based on structural biology using chitinase as a model to reinforce the role of giant viruses as a source of novel enzymes for biotechnological application.