Abstract
Heterocapsa circularisquama DNA virus (HcDNAV; previously designated as HcV) is a giant virus (girus) with a ~356-kbp double-stranded DNA (dsDNA) genome. HcDNAV lytically infects the bivalve-killing marine dinoflagellate H. circularisquama, and currently represents the sole DNA virus isolated from dinoflagellates, one of the most abundant protists in marine ecosystems. Its morphological features, genome type, and host range previously suggested that HcDNAV might be a member of the family Phycodnaviridae of Nucleo-Cytoplasmic Large DNA Viruses (NCLDVs), though no supporting sequence data was available. NCLDVs currently include two families found in aquatic environments (Phycodnaviridae, Mimiviridae), one mostly infecting terrestrial animals (Poxviridae), another isolated from fish, amphibians and insects (Iridoviridae), and the last one (Asfarviridae) exclusively represented by the animal pathogen African swine fever virus (ASFV), the agent of a fatal hemorrhagic disease in domestic swine. In this study, we determined the complete sequence of the type B DNA polymerase (PolB) gene of HcDNAV. The viral PolB was transcribed at least from 6 h post inoculation (hpi), suggesting its crucial function for viral replication. Most unexpectedly, the HcDNAV PolB sequence was found to be closely related to the PolB sequence of ASFV. In addition, the amino acid sequence of HcDNAV PolB showed a rare amino acid substitution within a motif containing highly conserved motif: YSDTDS was found in HcDNAV PolB instead of YGDTDS in most dsDNA viruses. Together with the previous observation of ASFV-like sequences in the Sorcerer II Global Ocean Sampling metagenomic datasets, our results further reinforce the ideas that the terrestrial ASFV has its evolutionary origin in marine environments.
Highlights
Heterocapsa circularisquama DNA virus (HcDNAV) is considered to play a significant role in the demise of H. circularisquama blooms [9,10]
HcDNAV is the sole DNA virus currently isolated from dinoflagellates, and to our knowledge, is the only DNA virus isolated from the superphylum Alveolata [12]
Based on its host range, genome type/size and microscopic features, HcDNAV was previously suggested to be a member of Phycodnaviridae [13]
Summary
Dinoflagellates (Dinophyceae) are one of the highly abundant and ubiquitous unicellular eukaryotic ("protistan") components in marine environments [1]. We aligned the HcDNAV PolB sequence with its homologs from NCLDVs. A phylogenetic tree based on the 362 amino acid residue sites from the alignment supported the monophyletic grouping of HcDNAV and ASFV with a 100% bootstrap value (Fig. 1). The resulting tree based on 320 amino acid residues again supported the grouping of HcDNAV/ASFV with a 98% bootstrap value (Fig. 2). A previous "phylogenetic mapping" survey of the metagenomic sequence data sets generated by the Global Ocean Sampling (GOS) expedition [31] revealed several PolBlike sequences most closely related to the PolB sequence of ASFV [32] This observation suggested the presence of ASFV-related viruses in marine environments. A phylogenetic tree using several environmental sequences supported their grouping with the terrestrial ASFV PolB (bootstrap value = 84%, Fig. 3). Exploring this hidden viral world is necessary to our understanding of the evolutionary relationships between aquatic viruses and their terrestrial relatives
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