High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

Abstract

Viruses belonging to the Nucleocytoviricota phylum are globally distributed and include members with notably large genomes with complex functional repertoires. Recent studies have shown that these viruses are particularly diverse and abundant in marine systems, but the magnitude of actively replicating Nucleocytoviricota present in ocean habitats remains unclear. In this study, we compiled a curated database of 2,431 Nucleocytoviricota genomes and used it to examine the gene expression of these viruses in a 2.5-day metatranscriptomic time-series from surface waters of the California Current. We identified 145 viral genomes with high levels of gene expression, including 90 Mimiviridae and 53 Phycodnaviridae. In addition to recovering high expression of core genes involved in information processing that are commonly expressed during viral infection, we also identified transcripts of diverse viral metabolic genes from pathways such as glycolysis, the TCA cycle, and the pentose phosphate pathway, suggesting that virus-mediated reprogramming of central carbon metabolism is common in oceanic surface waters. Surprisingly, we also identified viral transcripts with homology to actin, myosin, and kinesin domains, suggesting that viruses may use them to manipulate host cytoskeletal dynamics during infection. We performed phylogenetic analysis on the virus-encoded myosin and kinesin proteins, which demonstrated that most belong to deep-branching viral clades, but that others appear to have been acquired from eukaryotes more recently. Our results highlight a remarkable diversity of active Nucleocytoviricota in a coastal marine system and underscore the complex functional repertoires expressed by these viruses during infection.

A Phylogenomic Framework for Charting the Diversity and Evolution of Giant Viruses

“…The Algavirales is a sister lineage to the Imitervirales that contains 4 families encompassing several well-studied algal viruses. The Prasinoviridae (AG_01) is a family that includes viruses known to infect the prasinophyte genera Bathycoccus, Micromonas, and Ostreococcus [7], and cultivation-independent surveys have provided evidence that the MAGs in this clade are also associated with prasinophytes [36]. Similarly, our approach yielded a well-defined Phycodnaviridae family (AG_02) composed mostly of chloroviruses, consistent with the similar host range of these viruses [37].…”

Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton

“…We identified myosin-related genes in a total of 24 NCLDV MAGs (out of 2,275 considered in our survey) by performing BLASTP against reference myosin sequences compiled from a previous study ( Odronitz and Kollmar, 2007 ), through our own independent effort from a parallel environmental genomic survey ( Ha et al, 2021 ). These NCLDV MAGs were derived from the large cellular size fractions of Tara Oceans ( n = 10) and studies by Moniruzzaman et al (2020) ( n = 5) and Schulz et al (2020) ( n = 9).…”

Morphological and Genomic Features of the New Klosneuvirinae Isolate Fadolivirus IHUMI-VV54

“…This observation underlined the fact that viral production requires a greater production of energy by the infected cells. Further, active glycolysis and tricarboxylic acid cycles were identified by metagenomic studies (Moniruzzaman et al, 2020a;Ha et al, 2021) and some proteins were also found in Pandoravirus (Aherfi et al, 2020) and could have a confirmed functional activity such as the isocitrate dehydrogenase protein. Concerning the predicted ATPase subunit A, it is also present in some Klosneuvirinae.…”