The Giant Cafeteria roenbergensis Virus That Infects a Widespread Marine Phagocytic Protist Is a New Member of the Fourth Domain of Life

Philippe Colson,Mickaël Boyer,Ghislain Fournous,Gregory Gimenez,Didier Raoult,Jianming Qiu

doi:10.1371/journal.pone.0018935

Abstract

BackgroundA recent work has provided strong arguments in favor of a fourth domain of Life composed of nucleo-cytoplasmic large DNA viruses (NCLDVs). This hypothesis was supported by phylogenetic and phyletic analyses based on a common set of proteins conserved in Eukarya, Archaea, Bacteria, and viruses, and implicated in the functions of information storage and processing. Recently, the genome of a new NCLDV, Cafeteria roenbergensis virus (CroV), was released. The present work aimed to determine if CroV supports the fourth domain of Life hypothesis.MethodsA consensus phylogenetic tree of NCLDVs including CroV was generated from a concatenated alignment of four universal proteins of NCLDVs. Some features of the gene complement of CroV and its distribution along the genome were further analyzed. Phylogenetic and phyletic analyses were performed using the previously identified common set of informational genes present in Eukarya, Archaea, Bacteria, and NCLDVs, including CroV.FindingsPhylogenetic reconstructions indicated that CroV is clearly related to the Mimiviridae family. The comparison between the gene repertoires of CroV and Mimivirus showed similarities regarding the gene contents and genome organization. In addition, the phyletic clustering based on the comparison of informational gene repertoire between Eukarya, Archaea, Bacteria, and NCLDVs unambiguously classified CroV with other NCLDVs and clearly included it in a fourth domain of Life. Taken together, these data suggest that Mimiviridae, including CroV, may have inherited a common gene content probably acquired from a common Mimiviridae ancestor.ConclusionsThis further analysis of the gene repertoire of CroV consolidated the fourth domain of Life hypothesis and contributed to outline a functional pan-genome for giant viruses infecting phagocytic protistan grazers.

Highlights

In 2003, the discovery of Acanthamoeba polyphaga Mimivirus, which has the largest viral genome (1,18 kilobases) ever reported [1,2], gave a boost to knowledge and understanding in terms of the definition and origin of viruses [3,4]
Consensus phylogenetic tree of the nucleocytoplasmic large DNA viruses (NCLDVs) The phylogenetic tree of the NCLDVs based on a concatenated alignment of 4 universal NCVOGs indicated that Cafeteria roenbergensis virus (CroV) is related with the Mimiviridae family (Figure 1)
CroV is deeply positioned in the Mimiviridae branch, which contains a cluster formed by Mimivirus and all four close relative to Mimivirus isolated from Acanthamoeba spp. culture in our lab [18]

Summary

Introduction

In 2003, the discovery of Acanthamoeba polyphaga Mimivirus, which has the largest viral genome (1,18 kilobases (kb)) ever reported [1,2], gave a boost to knowledge and understanding in terms of the definition and origin of viruses [3,4]. Mimivirus has been suspected to constitute a fourth domain of Life, apart from bacteria, archaea and eukaryotes, based on the phylogeny of some of the Mimiviridae genes that are parts of a group of seven genes encoding universal proteins [2] This assumption has been vigorously debated though discussion of the appropriateness of genes used and the interpretation of phylogeny reconstructions [2,13,14,15,16,17]. A recent work has provided strong arguments in favor of a fourth domain of Life composed of nucleocytoplasmic large DNA viruses (NCLDVs) This hypothesis was supported by phylogenetic and phyletic analyses based on a common set of proteins conserved in Eukarya, Archaea, Bacteria, and viruses, and implicated in the functions of information storage and processing. The present work aimed to determine if CroV supports the fourth domain of Life hypothesis

Methods

Results

Conclusion