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Study of Gene Trafficking between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses.
Genome Biol Evol. 2016 12 14; 8(11):3351-3363.GB

Abstract

The nucleocytoplasmic large DNA viruses (NCLDV) are a group of extremely complex double-stranded DNA viruses, which are major parasites of a variety of eukaryotes. Recent studies showed that certain unicellular eukaryotes contain fragments of NCLDV DNA integrated in their genome, when surprisingly many of these organisms were not previously shown to be infected by NCLDVs. These findings prompted us to search the genome of Acanthamoeba castellanii strain Neff (Neff), one of the most prolific hosts in the discovery of giant NCLDVs, for possible DNA inserts of viral origin. We report the identification of 267 markers of lateral gene transfer with viruses, approximately half of which are clustered in Neff genome regions of viral origins, transcriptionally inactive or exhibit nucleotide-composition signatures suggestive of a foreign origin. The integrated viral genes had diverse origin among relatives of viruses that infect Neff, including Mollivirus, Pandoravirus, Marseillevirus, Pithovirus, and Mimivirus However, phylogenetic analysis suggests the existence of a yet-undiscovered family of amoeba-infecting NCLDV in addition to the five already characterized. The active transcription of some apparently anciently integrated virus-like genes suggests that some viral genes might have been domesticated during the amoeba evolution. These insights confirm that genomic insertion of NCLDV DNA is a common theme in eukaryotes. This gene flow contributed fertilizing the eukaryotic gene repertoire and participated in the occurrence of orphan genes, a long standing issue in genomics. Search for viral inserts in eukaryotic genomes followed by environmental screening of the original viruses should be used to isolate radically new NCLDVs.

Authors+Show Affiliations

URGI, INRA, Université Paris-Saclay, Versailles, France.Structural and Genomic Information Laboratory (IGS), Aix-Marseille Université, CNRS UMR (IMM FR 3479), Marseille, France guillaume.blanc@igs.cnrs-mrs.fr.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27811174

Citation

Maumus, Florian, and Guillaume Blanc. "Study of Gene Trafficking Between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses." Genome Biology and Evolution, vol. 8, no. 11, 2016, pp. 3351-3363.
Maumus F, Blanc G. Study of Gene Trafficking between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses. Genome Biol Evol. 2016;8(11):3351-3363.
Maumus, F., & Blanc, G. (2016). Study of Gene Trafficking between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses. Genome Biology and Evolution, 8(11), 3351-3363.
Maumus F, Blanc G. Study of Gene Trafficking Between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses. Genome Biol Evol. 2016 12 14;8(11):3351-3363. PubMed PMID: 27811174.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Study of Gene Trafficking between Acanthamoeba and Giant Viruses Suggests an Undiscovered Family of Amoeba-Infecting Viruses. AU - Maumus,Florian, AU - Blanc,Guillaume, Y1 - 2016/12/14/ PY - 2016/11/5/pubmed PY - 2017/9/28/medline PY - 2016/11/5/entrez KW - acanthamoeba KW - lateral gene transfer KW - nucleo-cytoplasmic large DNA virus SP - 3351 EP - 3363 JF - Genome biology and evolution JO - Genome Biol Evol VL - 8 IS - 11 N2 - The nucleocytoplasmic large DNA viruses (NCLDV) are a group of extremely complex double-stranded DNA viruses, which are major parasites of a variety of eukaryotes. Recent studies showed that certain unicellular eukaryotes contain fragments of NCLDV DNA integrated in their genome, when surprisingly many of these organisms were not previously shown to be infected by NCLDVs. These findings prompted us to search the genome of Acanthamoeba castellanii strain Neff (Neff), one of the most prolific hosts in the discovery of giant NCLDVs, for possible DNA inserts of viral origin. We report the identification of 267 markers of lateral gene transfer with viruses, approximately half of which are clustered in Neff genome regions of viral origins, transcriptionally inactive or exhibit nucleotide-composition signatures suggestive of a foreign origin. The integrated viral genes had diverse origin among relatives of viruses that infect Neff, including Mollivirus, Pandoravirus, Marseillevirus, Pithovirus, and Mimivirus However, phylogenetic analysis suggests the existence of a yet-undiscovered family of amoeba-infecting NCLDV in addition to the five already characterized. The active transcription of some apparently anciently integrated virus-like genes suggests that some viral genes might have been domesticated during the amoeba evolution. These insights confirm that genomic insertion of NCLDV DNA is a common theme in eukaryotes. This gene flow contributed fertilizing the eukaryotic gene repertoire and participated in the occurrence of orphan genes, a long standing issue in genomics. Search for viral inserts in eukaryotic genomes followed by environmental screening of the original viruses should be used to isolate radically new NCLDVs. SN - 1759-6653 UR - https://www.unboundmedicine.com/medline/citation/27811174/Study_of_Gene_Trafficking_between_Acanthamoeba_and_Giant_Viruses_Suggests_an_Undiscovered_Family_of_Amoeba_Infecting_Viruses_ L2 - https://academic.oup.com/gbe/article-lookup/doi/10.1093/gbe/evw260 DB - PRIME DP - Unbound Medicine ER -