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Welcome to pandoraviruses at the 'Fourth TRUC' club.

ABSTRACT: Nucleocytoplasmic large DNA viruses, or representatives of the proposed order Megavirales, belong to families of giant viruses that infect a broad range of eukaryotic hosts. Megaviruses have been previously described to comprise a fourth monophylogenetic TRUC (things resisting uncompleted classification) together with cellular domains in the universal tree of life. Recently described pandoraviruses have large (1.9-2.5 MB) and highly divergent genomes. In the present study, we updated the classification of pandoraviruses and other reported giant viruses. Phylogenetic trees were constructed based on six informational genes. Hierarchical clustering was performed based on a set of informational genes from Megavirales members and cellular organisms. Homologous sequences were selected from cellular organisms using TimeTree software, comprising comprehensive, and representative sets of members from Bacteria, Archaea, and Eukarya. Phylogenetic analyses based on three conserved core genes clustered pandoraviruses with phycodnaviruses, exhibiting their close relatedness. Additionally, hierarchical clustering analyses based on informational genes grouped pandoraviruses with Megavirales members as a super group distinct from cellular organisms. Thus, the analyses based on core conserved genes revealed that pandoraviruses are new genuine members of the 'Fourth TRUC' club, encompassing distinct life forms compared with cellular organisms.

SUBMITTER: Sharma V

PROVIDER: S-EPMC4435241 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Welcome to pandoraviruses at the 'Fourth TRUC' club.

Sharma Vikas V Colson Philippe P Chabrol Olivier O Scheid Patrick P Pontarotti Pierre P Raoult Didier D

Frontiers in microbiology 20150518

Nucleocytoplasmic large DNA viruses, or representatives of the proposed order Megavirales, belong to families of giant viruses that infect a broad range of eukaryotic hosts. Megaviruses have been previously described to comprise a fourth monophylogenetic TRUC (things resisting uncompleted classification) together with cellular domains in the universal tree of life. Recently described pandoraviruses have large (1.9-2.5 MB) and highly divergent genomes. In the present study, we updated the classif ...[more]

PMID: 26042093

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Project description: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.

Project description:Giant viruses are complex members of the virosphere, exhibiting outstanding structural and genomic features. Among these viruses, the pandoraviruses are some of the most intriguing members, exhibiting giant particles and genomes presenting at up to 2.5?Mb, with many genes having no known function. In this work, we analyzed, by virological and microscopic methods, the replication cycle steps of three new pandoravirus isolates from samples collected in different regions of Brazil. Our data indicate that all analyzed pandoravirus isolates can deeply modify the Acanthamoeba cytoplasmic environment, recruiting mitochondria and membranes into and around the electron-lucent viral factories. We also observed that the viral factories start forming before the complete degradation of the cellular nucleus. Various patterns of pandoravirus particle morphogenesis were observed, and the assembly of the particles seemed to be started either by the apex or by the opposite side. On the basis of the counting of viral particles during the infection time course, we observed that pandoravirus particles could undergo exocytosis after their morphogenesis in a process that involved intense recruitment of membranes that wrapped the just-formed particles. The treatment of infected cells with brefeldin affected particle exocytosis in two of the three analyzed strains, indicating biological variability among isolates. Despite such particle exocytosis, the lysis of host cells also contributed to viral release. This work reinforces knowledge of and reveals important steps in the replication cycle of pandoraviruses.IMPORTANCE The emerging Pandoraviridae family is composed of some of the most complex viruses known to date. Only a few pandoravirus isolates have been described until now, and many aspects of their life cycle remain to be elucidated. A comprehensive description of the replication cycle is pivotal to a better understanding of the biology of the virus. For this report, we describe new pandoraviruses and used different methods to better characterize the steps of the replication cycle of this new group of viruses. Our results provide new information about the diversity and biology of these giant viruses.

Project description:Giant viruses of amoebae are distinct from classical viruses by the giant size of their virions and genomes. Pandoraviruses are the record holders in size of genomes and number of predicted genes. Three strains, P. salinus, P. dulcis, and P. inopinatum, have been described to date. We isolated three new ones, namely P. massiliensis, P. braziliensis, and P. pampulha, from environmental samples collected in Brazil. We describe here their genomes, the transcriptome and proteome of P. massiliensis, and the pangenome of the group encompassing the six pandoravirus isolates. Genome sequencing was performed with an Illumina MiSeq instrument. Genome annotation was performed using GeneMarkS and Prodigal softwares and comparative genomic analyses. The core genome and pangenome were determined using notably ProteinOrtho and CD-HIT programs. Transcriptomics was performed for P. massiliensis with the Illumina MiSeq instrument; proteomics was also performed for this virus using 1D/2D gel electrophoresis and mass spectrometry on a Synapt G2Si Q-TOF traveling wave mobility spectrometer. The genomes of the three new pandoraviruses are comprised between 1.6 and 1.8 Mbp. The genomes of P. massiliensis, P. pampulha, and P. braziliensis were predicted to harbor 1,414, 2,368, and 2,696 genes, respectively. These genes comprise up to 67% of ORFans. Phylogenomic analyses showed that P. massiliensis and P. braziliensis were more closely related to each other than to the other pandoraviruses. The core genome of pandoraviruses comprises 352 clusters of genes, and the ratio core genome/pangenome is less than 0.05. The extinction curve shows clearly that the pangenome is still open. A quarter of the gene content of P. massiliensis was detected by transcriptomics. In addition, a product for a total of 162 open reading frames were found by proteomic analysis of P. massiliensis virions, including notably the products of 28 ORFans, 99 hypothetical proteins, and 90 core genes. Further analyses should allow to gain a better knowledge and understanding of the evolution and origin of these giant pandoraviruses, and of their relationships with viruses and cellular microorganisms.

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Welcome to pandoraviruses at the 'Fourth TRUC' club.

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Welcome to pandoraviruses at the 'Fourth TRUC' club.

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