Abstract
Since the discovery of Mimivirus, viruses with large genomes encoding components of the translation machinery and other cellular processes have been described as belonging to the nucleocytoplasmic large DNA viruses. Recently, genome-resolved metagenomics led to the discovery of more than 40 viruses that have been grouped together in a proposed viral subfamily named Klosneuvirinae. Members of this group had genomes of up to 2.4Mb in size and featured an expanded array of translation system genes. Yet, despite the large diversity of the Klosneuvirinae in metagenomic data, there are currently only two isolates available. Here, we report the isolation of a novel giant virus known as Fadolivirus from an Algerian sewage site and provide morphological data throughout its replication cycle in amoeba and a detailed genomic characterization. The Fadolivirus genome, which is more than 1.5Mb in size, encodes 1,452 predicted proteins and phylogenetic analyses place this viral isolate as a near relative of the metagenome assembled Klosneuvirus and Indivirus. The genome encodes for 66 tRNAs, 23 aminoacyl-tRNA synthetases and a wide range of transcription factors, surpassing Klosneuvirus and other giant viruses. The Fadolivirus genome also encodes putative vacuolar-type proton pumps with the domains D and A, potentially constituting a virus-derived system for energy generation. The successful isolation of Fadolivirus will enable future hypothesis-driven experimental studies providing deeper insights into the biology of the Klosneuvirinae.
Highlights
In 2003, with the first description of Mimivirus (La Scola, 2003), viruses were revealed to be more complex entities than previously thought and with extraordinary properties, e.g., numerous tRNAs, aminoacyl-tRNA synthetases and themselves being infected by virophages (La Scola et al, 2008; Gaia et al, 2014)
Its replicative cycle in V. vermiformis is comparable to other NCLDVs that have been described, such as Yasminevirus (Bajrai et al, 2019)
Fadolivirus shows significant proximity to Klosneuvirus KNV1, virus described by a previous metagenomic study (Schulz et al, 2017), by phylogenetic analysis and by genomic comparison
Summary
In 2003, with the first description of Mimivirus (La Scola, 2003), viruses were revealed to be more complex entities than previously thought and with extraordinary properties, e.g., numerous tRNAs, aminoacyl-tRNA synthetases (aaRS) and themselves being infected by virophages (La Scola et al, 2008; Gaia et al, 2014). The description of Meelsvirus revealed that these potential viruses can take extremely varied forms and are associated with a complex formation of their capsids (Shinn and Bullard, 2018). These large viruses share a common origin and a novel name has been proposed: Nucleocytoviricota (replacing the term nucleocytoplasmic large DNA viruses (NCLDV; Koonin et al, 2020). Just 1 year later, the diversity of this unexplored viral group was further expanded with the discovery of seven additional metagenome assembled viruses from soil (Schulz et al, 2018) and the first isolate affiliated with the Klosneuvirinae, Bodo saltans virus (Deeg et al, 2018). Metagenomic has revealed the widespread presence of energy metabolism encoded in the Nucleocytoviricota, such as photosynthesis genes and enzymes playing roles in glycolysis among others (Schulz et al, 2020; Moniruzzaman et al, 2020a)
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