Abstract

BackgroundTransposable 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.ResultsHerein, 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.ConclusionsOur 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.

Highlights

  • Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes

  • We focused on miniature inverted-repeat transposable elements (MITEs) because their small size may allow a long-term persistence in diverse lineages through evasion of the host defense system2 and because a substantial number of one MITE belonging to the Tc1/mariner superfamily has been found in the genome of a giant virus, P. salinus [6]

  • These repeats shared all features reported for MITEs (3), including a small size (116–422-bp), terminal inverted repeats (TIRs), 2–8-bp target site duplication (TSD), stable secondary structure, lack of coding capacity and high size homogeneity (Additional file 1: Table S1 and Additional file 3: Figure S1a,d)

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Summary

Introduction

Transposable elements (TEs) are common and often present with high copy numbers in cellular genomes. Transposable elements (TEs) are DNA fragments that can move from one place to another in their host genomes, often resulting in their own amplification in the process [1]. DNA transposons represent a specific group of TEs, and they can be classified as either “autonomous” or “non-autonomous” elements. Autonomous transposons can transpose by themselves, while non-autonomous elements require enzymes encoded in trans by autonomous elements to be mobile [2]. Miniature inverted–repeat transposable elements (MITEs) are non-autonomous elements typically showing high copy numbers and length homogeneity [3, 4]. MITEs form several superfamilies classified according to sequence similarity between their TIRs or TSD and those of autonomous partners. It has been shown that MITEs play important roles in eukaryotic evolution, including an increase in genome size, formation of new genes, and the regulation of gene expression [5,6,7,8]

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