Abstract
Viruses have long been viewed as entities possessing extremely limited metabolic capacities. Over the last decade, however, this view has been challenged, as metabolic genes have been identified in viruses possessing large genomes and virions-the synthesis of which is energetically demanding. Here, we unveil peculiar phenotypic and genomic features of Prymnesium kappa virus RF01 (PkV RF01), a giant virus of the Mimiviridae family. We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, such as all four succinate dehydrogenase (SDH) subunits (A-D) as well as key enzymes in the β-oxidation pathway. The SDHA gene was transcribed upon infection, indicating that the viral SDH is actively used by the virus- potentially to modulate its host's energy metabolism. We detected orthologous SDHA and SDHB genes in numerous genome fragments from uncultivated marine Mimiviridae viruses, which suggests that the viral SDH is widespread in oceans. PkV RF01 was less virulent compared with other cultured prymnesioviruses, a phenomenon possibly linked to the metabolic capacity of this virus and suggestive of relatively long co-evolution with its hosts. It also has a unique morphology, compared to other characterized viruses in the Mimiviridae family. Finally, we found that PkV RF01 is the only alga-infecting Mimiviridae virus encoding two aminoacyl-tRNA synthetases and enzymes corresponding to an entire base-excision repair pathway, as seen in heterotroph-infecting Mimiviridae These Mimiviridae encoded-enzymes were found to be monophyletic and branching at the root of the eukaryotic tree of life. This placement suggests that the last common ancestor of Mimiviridae was endowed with a large, complex genome prior to the divergence of known extant eukaryotes.IMPORTANCE 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 Prymnesium kappa virus RF01, a large alga-infecting virus with a unique morphology, an atypical infection profile, and an unprecedented number of genes involved in energy metabolism (such as the tricarboxylic (TCA) cycle and the β-oxidation pathway). Moreover, 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 has the potential to actively regulate energy metabolism with its own gene.
Highlights
Viruses have long been viewed as entities possessing extremely limited metabolic capacities
FCM, flow cytometry. bThe number of viral particles released from each host cell, estimated from the total number of host cells preinfection and the total number of virus-like particles (VLPs) produced during the infection cycle. cEstimated as the percentage of infectious progeny of all VLPs produced during the infection cycle. dNumber of infectious particles released per host cell. eMPN, most probable number
We reported recently that the PkV RF01 genome has additional nucleocytoplasmic large DNA virus (NCLDV) core genes, such as A32-like virion packing ATPase and RNApol (RNA pol subunit I [NCVOG0274] and subunit II [NCVOG0271]), and orthologous genes that are specific to Mimiviridae, namely, MutS7 (NCVOG2626) and asparagine synthase (AsnS; NCVOG0061) [60]
Summary
Viruses have long been viewed as entities possessing extremely limited metabolic capacities. We unveil peculiar phenotypic and genomic features of Prymnesium kappa virus RF01 (PkV RF01), a giant virus of the Mimiviridae family We found that this virus encodes an unprecedented number of proteins involved in energy metabolism, including all four succinate dehydrogenase (SDH) subunits (A to D), as well as key enzymes in the b-oxidation pathway. PkV RF01 was less virulent than other cultured prymnesioviruses, a phenomenon that may be linked to the metabolic capacity of this virus and is suggestive of relatively long coevolution with its hosts It has a unique morphology compared to those of other characterized viruses in the Mimiviridae family. We report new phenotypic features, as well as new viral functions inferred from analysis of the genome sequence of PkV RF01 We found that this virus has a unique morphology, is less virulent than most other alga-infecting viruses, and possesses an unprecedented number of energy-generating genes. Our findings of peculiar genomic features in a persistent virus provide new insights on virus-host coevolution and may stimulate further advances in modeling the history of their interaction
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