Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements

Abstract

Background: Tc1/mariner transposons are widespread DNA transposable elements (TEs) that have made important contributions to the evolution of host genomic complexity in metazoans. However, the evolution and diversity of the Tc1/mariner superfamily remains poorly understood. Following recent developments in genome sequencing and the availability of a wealth of new genomes, Tc1/mariner TEs have been identified in many new taxa across the eukaryotic tree of life. To date, the majority of studies focussing on Tc1/mariner elements have considered only a single host lineage or just a small number of host lineages. Thus, much remains to be learnt about the evolution of Tc1/mariner TEs by performing analyses that consider elements that originate from across host diversity. Results: We mined the non-redundant database of NCBI using BLASTp searches, with transposase sequences from a diverse set of reference Tc1/mariner elements as queries. A total of 5158 Tc1/mariner elements were retrieved and used to reconstruct evolutionary relationships within the superfamily. The resulting phylogeny is well resolved and includes several new groups of Tc1/mariner elements. In particular, we identify a new family of plant-genome restricted Tc1/mariner elements, which we call PlantMar. We also show that the pogo family is much larger and more diverse than previously appreciated, and we review evidence for a potential revision of its status to become a separate superfamily. Conclusions: Our study provides an overview of Tc1-mariner phylogeny and summarises the impressive diversity of Tc1-mariner TEs among sequenced eukaryotes. Tc1/mariner TEs are successful in a wide range of eukaryotes, especially unikonts (the taxonomic supergroup containing Amoebozoa, Opisthokonta, Breviatea, and Apusomonadida). In particular, ecdysozoa, and especially arthropods, emerge as important hosts for Tc1/mariner elements (except the PlantMar family). Meanwhile, the pogo family, which is by far the largest Tc1/mariner family, also includes many elements from fungal and chordate genomes. Moreover, there is evidence of the repeated exaptation of pogo elements in vertebrates, including humans, in addition to the well-known example of CENP-B. Collectively, our findings provide a considerable advancement in understanding of Tc1/mariner elements, and more generally they suggest that much work remains to improve understanding of the diversity and evolution of DNA TEs.

Network‐based visualisation reveals new insights into transposable element diversity

“…We first applied our method to alignments between transposable elements drawn from the Tc1/mariner superfamily. We chose this TE family due to its wide phylogenetic distribution (Dupeyron et al, 2020), and because Tc1/mariner elements are well characterised as active TEs in C. elegans (Bessereau, 2006). We constructed a network in which each individual TE is a separate node and the weight of the connection between each node is determined by the sequence similarity.…”

“…As an example, we selected one of these clusters, mc476, which was composed of two subfamilies annotated by our pipeline as Fot1 and Tc1 (Fig 2D). Fot1 TEs are most common in fungi, although some metazoan examples have been found (Dupeyron et al, 2020). The origin of this element in nematodes is thus unknown.…”

Broadscale evolutionary analysis of eukaryotic DDE transposons

“…We included transposases from all DDE superfamilies in our analyses, updating the 17 superfamily framework of Yuan and Wessler (13), i.e. Tc1/mariner, Merlin, PIF/Harbinger, MULE (Mutator + Rehavkus), P, hAT, Kolobok, Novosib, Sola1, Sola2, Sola3, PiggyBac, CMC (CACTA, Mirage, Chapaev), Transib, Academ, Ginger, Zator , to include a total of 19 superfamilies, with the follow changes in line with recent research: (i) we split Pogo from Tc1/mariner to form its own distinct superfamily (59, 60) (ii); we grouped PIF/Harbinger with Spy as the superfamily PHIS (61); (iii) we included the newly described GingerRoot family (62).…”

“…We used the transposase amino acid sequences from Yuan and Wessler (13) for our database searches, except for MULE, Pogo, Tc1/mariner , and GingerRoot, where we used sequences from more recent analyses (53, 54, 62). We queried the NCBI nr database with BLASTp (63, 64), using a script to parse outputs, specifying table format output, including a column containing the subject sequence.…”

Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons

“…Nine families are classically considered, and most of their phylogenetic relationships have been updated and are well defined: DD34E/Tc1 [25], DD34D/mariner [26], DD37D/maT [23], DD39D/GT [23], DD41D/VS [24], DD35E/TR [20], DD36E/IC [21], DD37E/TRT [27] and DD38E/IT [22]. However, until recently, studies have shown that many groups of ITm transposons carry the same DDE/D signatures but have different phylogenetic origins [28][29][30]. In particular, the DD34E/Gambol [31] and DDxD/pogo [30] transposons, which were designated as the Tc1/mariner superfamily, have been shown to form two separate superfamilies with good bootstrap support [30].…”