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

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.

Keywords: Autonomous partner; Genome evolution; Horizontal transfer; MITEs; Virus.

Fig. 1

The schematic representation of phylogenetic relationships of viruses. The presence of MITEs in viral genomes is shown using rectangles. Species abbreviations were shown in Additional file 1: Table S1

Fig. 2

Copy number and content of ten MITEs in the viral genomes. a Comparison of copy numbers of ten MITEs in studied viruses. b Amount of nucleotide covered by each MITE in five viral genomes

Fig. 3

Multiple alignments of the 5′ and 3′ terminal sequences of hAT-NA1 to hAT-NA5 (a and b), hATm-NA6 (c), Submariner-NA (d), IS200/IS605_NA (e) and CMC-NA (f) with their corresponding potential autonomous elements. MITEs identified in viruses are shown using red color. Species abbreviations are shown in Additional file 1: Table S1. CfTEC was obtained from the previous report [26], and the rest of the CACTA transposons were retrieved from Repbase [20]. TIRs of hATm-6_RP and hATm-6_CV are 417 bp and 575 bp, respectively. Therefore, only 40 bp of both termini of these transposons are shown using arrows

Fig. 4

Dotplot comparsions of seven MITEs involved in HTs between viruses and its potential hosts. Species abbreviations were shown in Additional file 1: Table S1, and multiple alignments of these MITEs were indicated in Additional file 9: Figure S5

Fig. 5

The phylogenetic relationship of two MITEs from viral and host genomes. a A phylogenetic tree of full-length copies of Submariner-NA elements from pandoraviruses and their host amoeba. b Phylogeny of full-length copies of hAT-NA5 elements from pandoraviruses and their host amoeba. Clade credibility values (> 70%) are shown at each node. Each intact copy from different species is indicated using distinguishable color lines. Because hAT-NA5 from A. castellanii and A. pearcei are identical, and they are displayed using fluorescent green lines