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1. Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes

Author

Hua-Hao Zhang, Qiu-Zhong Zhou, Ping-Lan Wang, Xiao-Min Xiong, Andrea Luchetti, Didier Raoult, Anthony Levasseur, Sebastien Santini, Chantal Abergel, Matthieu Legendre, Jean-Michel Drezen, Catherine Béliveau, Michel Cusson, Shen-Hua Jiang, Hai-Ou Bao, Cheng Sun, Thomas E. Bureau, Peng-Fei Cheng, Min-Jin Han, Ze Zhang, Xiao-Gu Zhang, and Fang-Yin Dai

Subjects
Virus, MITEs, Autonomous partner, Horizontal transfer, Genome evolution, Genetics, QH426-470
Abstract

Abstract Background Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes. Unlike in cellular organisms, TEs were previously thought to be either rare or absent in viruses. Almost all reported TEs display only one or two copies per viral genome. In addition, the discovery of pandoraviruses with genomes up to 2.5-Mb emphasizes the need for biologists to rethink the fundamental nature of the relationship between viruses and cellular life. Results Herein, we performed the first comprehensive analysis of miniature inverted-repeat transposable elements (MITEs) in the 5170 viral genomes for which sequences are currently available. Four hundred and fifty one copies of ten miniature inverted-repeat transposable elements (MITEs) were found and each MITE had reached relatively large copy numbers (some up to 90) in viruses. Eight MITEs belonging to two DNA superfamilies (hobo/Activator/Tam3 and Chapaev–Mirage–CACTA) were for the first time identified in viruses, further expanding the organismal range of these two superfamilies. TEs may play important roles in shaping the evolution of pandoravirus genomes, which were here found to be very rich in MITEs. We also show that putative autonomous partners of seven MITEs are present in the genomes of viral hosts, suggesting that viruses may borrow the transpositional machinery of their cellular hosts’ autonomous elements to spread MITEs and colonize their own genomes. The presence of seven similar MITEs in viral hosts, suggesting horizontal transfers (HTs) as the major mechanism for MITEs propagation. Conclusions Our discovery highlights that TEs contribute to shape genome evolution of pandoraviruses. We concluded that as for cellular organisms, TEs are part of the pandoraviruses’ diverse mobilome.

Published
2018
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2. Unexpected invasion of miniature inverted-repeat transposable elements in viral genomes

Author

Ze Zhang, Min-Jin Han, Shen-Hua Jiang, Ping-Lan Wang, Xiao-Min Xiong, Qiu-Zhong Zhou, Jean-Michel Drezen, Xiao-Gu Zhang, Didier Raoult, Michel Cusson, Chantal Abergel, Cheng Sun, Matthieu Legendre, Anthony Levasseur, Thomas E. Bureau, Sébastien Santini, Andrea Luchetti, Catherine Béliveau, Fang-Yin Dai, Hua-Hao Zhang, Peng-Fei Cheng, Hai-Ou Bao, Zhang, Hua-Hao, Zhou, Qiu-Zhong, Wang, Ping-Lan, Xiong, Xiao-Min, Luchetti, Andrea, Raoult, Didier, Levasseur, Anthony, Santini, Sebastien, Abergel, Chantal, Legendre, Matthieu, Drezen, Jean-Michel, Béliveau, Catherine, Cusson, Michel, Jiang, Shen-Hua, Bao, Hai-Ou, Sun, Cheng, Bureau, Thomas E., Cheng, Peng-Fei, Han, Min-Jin, Zhang, Ze, Zhang, Xiao-Gu, Dai, Fang-Yin, College of Pharmacy and Life Science [Jiujiang, China], Jiujiang University [China], State Key Laboratory of Silkworm Genome Biology & Key Laboratory of Sericultural Biology and Genetic Breeding [Chongqing, China], Southwest University [Chongqing]-Ministry of Agriculture [Chongqing, China], School of Life Sciences [Chongqing, China], Chongqing University [Chongqing], Clinical Medical College [Jiujiang, China], Dipartimento di Scienze Biologiche, Geologiche e Ambientali [Bologna, Italy], Alma Mater Studiorum Università di Bologna [Bologna] (UNIBO), Unité des Rickettsies et pathogènes émergents (URPE), Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48, Institut des sciences biologiques (INSB-CNRS)-Institut des sciences biologiques (INSB-CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48, Institut des sciences biologiques (INSB-CNRS)-Institut des sciences biologiques (INSB-CNRS)-Centre National de la Recherche Scientifique (CNRS), Information génomique et structurale (IGS), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Laurentian Forestry Centre, Natural Resources Canada (NRCan), Institute of Apicultural Research [Beijing, China], Chinese Academy of Agricultural Sciences (CAAS), Department of Biology [Montréal], McGill University = Université McGill [Montréal, Canada], Poyang Lake Eco-economy Research Center [Jiujiang, China], This work was supported by the National Natural Science Foundation of China (31560308 and 31700318 to H.H.Z, 31471197 to Z.Z.), the Hi-Tech Research and Development 863 Program of China (2013AA102507 to F.Y.D.), the Natural Science Foundation of Jiangxi Province (20171BAB204016 to H.H.Z.) and State Key Laboratory of Silkworm Genome Biology (sklsgb161718–8 to H.H.Z)., Poirot, Olivier, INSB-INSB-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48, INSB-INSB-Centre National de la Recherche Scientifique (CNRS), and Université de Tours-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, Transposable element, Genome evolution, lcsh:QH426-470, Inverted repeat, 030106 microbiology, Horizontal transfer, Biology, Genome, MITEs, 03 medical and health sciences, Mite, Molecular Biology, [SDV.MP.VIR] Life Sciences [q-bio]/Microbiology and Parasitology/Virology, MITE, Pandoravirus, Research, Viru, biology.organism_classification, Virus, lcsh:Genetics, 030104 developmental biology, Evolutionary biology, Horizontal gene transfer, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, Mobilome, Autonomous partner
Abstract

Background Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes. Unlike in cellular organisms, TEs were previously thought to be either rare or absent in viruses. Almost all reported TEs display only one or two copies per viral genome. In addition, the discovery of pandoraviruses with genomes up to 2.5-Mb emphasizes the need for biologists to rethink the fundamental nature of the relationship between viruses and cellular life. Results Herein, we performed the first comprehensive analysis of miniature inverted-repeat transposable elements (MITEs) in the 5170 viral genomes for which sequences are currently available. Four hundred and fifty one copies of ten miniature inverted-repeat transposable elements (MITEs) were found and each MITE had reached relatively large copy numbers (some up to 90) in viruses. Eight MITEs belonging to two DNA superfamilies (hobo/Activator/Tam3 and Chapaev–Mirage–CACTA) were for the first time identified in viruses, further expanding the organismal range of these two superfamilies. TEs may play important roles in shaping the evolution of pandoravirus genomes, which were here found to be very rich in MITEs. We also show that putative autonomous partners of seven MITEs are present in the genomes of viral hosts, suggesting that viruses may borrow the transpositional machinery of their cellular hosts’ autonomous elements to spread MITEs and colonize their own genomes. The presence of seven similar MITEs in viral hosts, suggesting horizontal transfers (HTs) as the major mechanism for MITEs propagation. Conclusions Our discovery highlights that TEs contribute to shape genome evolution of pandoraviruses. We concluded that as for cellular organisms, TEs are part of the pandoraviruses’ diverse mobilome. Electronic supplementary material The online version of this article (10.1186/s13100-018-0125-4) contains supplementary material, which is available to authorized users.

Published
2018
Full Text
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