A persistent giant algal virus, with a unique morphology, encodes an unprecedented number of genes involved in energy metabolism

Abstract

Viruses on Earth are tremendously diverse in terms of morphology, functionality, and genomic composition. Over the last decade, the conceptual gap separating viruses and cellular life has tightened because of the detection of metabolic genes in viral genomes that express complex virus phenotypes upon infection. Here, we describe the 1.4 MB linear genome of Prymnesium kappa Virus RF01 (PkV RF01), a large alga-infecting virus of the Mimiviridae family with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic acid cycle (TCA) cycle and the β-oxidation pathway). We show that the gene corresponding to one of these enzymes (the succinate dehydrogenase subunit A) is transcribed during infection and is widespread among marine viruses. This discovery provides evidence that a virus can actively regulate energy metabolism with its own gene.

Host Range and Coding Potential of Eukaryotic Giant Viruses

“…It was further proposed that these viruses should form part of an extended Mimiviridae [ 11 , 13 , 42 , 74 , 75 ] or even the subfamily Mesomimivirinae within Mimiviridae [ 42 , 43 , 76 ] ( Figure 1 ). Mesomimivirinae is certainly expanding as most newly reported alga-infecting viruses join this clade instead of Phycodnaviridae , such as the viruses from Florenciella , Rhizochromulina , a chlorarachniophyte, and Prymnesium kappa [ 51 , 52 , 77 ] (not shown in Figure 1 ). These, plus the viruses of heterotrophic flagellates Cafeteria , Bodo , and Bicosta , all transform Mimiviridae into a more non-amoebal virus family.…”

“…Giant viruses exert control over different levels of genetic information in a cell. In addition to their own DNA polymerase and ligase for genome replication, some giant viruses encode DNA glycosylase involved in base excision repair pathways that could potentially remove damages to their large genomes [ 77 , 99 ]. Most NCLDVs also encode DNA-dependent RNA polymerase (DDRP) subunits ( Table 1 ) with architectural modifications that confer them higher speed and processivity than the cellular homologs [ 54 ].…”

“…Such control can be transcriptional regulation of nucleus- and mitochondrion-encoded genes related to energy metabolism, as in coccolithovirus [ 129 ]. Recently reported genome sequences of environmental MAGs [ 17 ] or isolated viruses even encode their own genes related to glycolysis, tricarboxylic acid cycle, succinate dehydrogenase, β-oxidation, and photosynthesis [ 17 , 77 , 81 , 101 ]. Genes encoding enzymes in cellular fermentation, such as pyruvate formate-lyase, have been found in Tetraselmis virus infecting green algae [ 73 ], which have anaerobic energy metabolism in low-oxygen condition [ 130 ].…”

Year-round dynamics of amplicon sequence variant communities differ among eukaryotes,Mimiviridae, and prokaryotes in a coastal ecosystem

“…The lower recurrence and persistence of Mimiviridae ASVs than eukaryote ASVs may be due to the existence of multiple Mimiviridae that can infect the same host species. A recent study suggested that Mimiviridae that infect K -strategist eukaryotes have long infection and latent periods to maximize the chance of vertical transmission, since the chances of horizontal transmissions are low due to the low host density (44). Viruses of K -strategist eukaryotes are more likely to exist inside the host cell (i.e., a long latent period), while viruses of r -strategist eukaryotes are more likely to be found outside their host (i.e., they show higher virulence and tend to produce virions more quickly) (44).…”

“…A recent study suggested that Mimiviridae that infect K -strategist eukaryotes have long infection and latent periods to maximize the chance of vertical transmission, since the chances of horizontal transmissions are low due to the low host density (44). Viruses of K -strategist eukaryotes are more likely to exist inside the host cell (i.e., a long latent period), while viruses of r -strategist eukaryotes are more likely to be found outside their host (i.e., they show higher virulence and tend to produce virions more quickly) (44). The size fraction we used for the detection of viral sequences (0.2–0.8 μm) may be enriched in free virions, which might have led to the preferential detection of r -strategist Mimiviridae .…”