Abstract
Giant viruses of amoebae were discovered in 2003. Since then, their diversity has greatly expanded. They were suggested to form a fourth branch of life, collectively named ‘TRUC’ (for “Things Resisting Uncompleted Classifications”) alongside Bacteria, Archaea, and Eukarya. Their origin and ancestrality remain controversial. Here, we specify the evolution and definition of giant viruses. Phylogenetic and phenetic analyses of informational gene repertoires of giant viruses and selected bacteria, archaea and eukaryota were performed, including structural phylogenomics based on protein structural domains grouped into 289 universal fold superfamilies (FSFs). Hierarchical clustering analysis was performed based on a binary presence/absence matrix constructed using 727 informational COGs from cellular organisms. The presence/absence of ‘universal’ FSF domains was used to generate an unrooted maximum parsimony phylogenomic tree. Comparison of the gene content of a giant virus with those of a bacterium, an archaeon, and a eukaryote with small genomes was also performed. Overall, both cladistic analyses based on gene sequences of very central and ancient proteins and on highly conserved protein fold structures as well as phenetic analyses were congruent regarding the delineation of a fourth branch of microbes comprised by giant viruses. Giant viruses appeared as a basal group in the tree of all proteomes. A pangenome and core genome determined for Rickettsia bellii (bacteria), Methanomassiliicoccus luminyensis (archaeon), Encephalitozoon intestinalis (eukaryote), and Tupanvirus (giant virus) showed a substantial proportion of Tupanvirus genes that overlap with those of the cellular microbes. In addition, a substantial genome mosaicism was observed, with 51, 11, 8, and 0.2% of Tupanvirus genes best matching with viruses, eukaryota, bacteria, and archaea, respectively. Finally, we found that genes themselves may be subject to lateral sequence transfers. In summary, our data highlight the quantum leap between classical and giant viruses. Phylogenetic and phyletic analyses and the study of protein fold superfamilies confirm previous evidence of the existence of a fourth TRUC of life that includes giant viruses, and highlight its ancestrality and mosaicism. They also point out that best evolutionary representations for giant viruses and cellular microorganisms are rhizomes, and that sequence transfers rather than gene transfers have to be considered.
Highlights
Since the Mimivirus discovery in 2003, dozens of giant viruses that infect Acanthamoeba spp. or Vermamoeba vermiformis have been isolated from various environmental samples, and more recently from animals including humans (La Scola et al, 2003; Raoult et al, 2004; Colson et al, 2017a)
Protein sequences from completely-sequenced proteomes of 80 Megavirales were scanned against the library of hidden Markov models (HMMs) of structural recognition maintained by the SUPERFAMILY database for structure assignment at an E-value cutoff of < 0.0001 (Gough et al, 2001; Gough and Chothia, 2002)
The late arrival of modern genetics ∼3 billion years (Gy) ago signals the end of a period responsible for the primordial cellular origin of viruses, clearly evident by the fact that the oldest superfamilies are common to cells and viruses (Nasir and Caetano-Anollés, 2015)
Summary
Since the Mimivirus discovery in 2003, dozens of giant viruses that infect Acanthamoeba spp. or Vermamoeba vermiformis have been isolated from various environmental samples, and more recently from animals including humans (La Scola et al, 2003; Raoult et al, 2004; Colson et al, 2017a). Families Mimiviridae (La Scola et al, 2005) and Marseilleviridae (Boyer et al, 2009; Colson et al, 2013b) and isolates that represent new putative families of giant viruses of amoebae, including pandoraviruses (Philippe et al, 2013), pithoviruses (Legendre et al, 2015), faustoviruses (Reteno et al, 2015), Mollivirus (Legendre et al, 2015), Kaumoebavirus (Bajrai et al, 2016), cedratviruses (Andreani et al, 2016), Pacmanvirus (Andreani et al, 2017), and Orpheovirus (Andreani et al, 2018) have been described (Colson et al, 2017b) These giant viruses of amoebae exhibit unique phenotypic and genotypic characteristics that differentiate them from ‘traditional’ viruses and bring them close to small microbes (Lwoff, 1957; Colson et al, 2017a). Together with a common virion architecture and common major biological features including reproduction within cytoplasmic factories, this contributed to propose reclassifying NCLDVs, mimiviruses and marseilleviruses in a new viral order named Megavirales (Colson et al, 2013a)
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