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Article

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

by
Shasha Shi
1,†,
Mikhail Puzakov
2,†,
Zhongxia Guan
1,
Kuilin Xiang
1,
Mohamed Diaby
1,
Yali Wang
1,
Saisai Wang
1,
Chengyi Song
1 and
Bo Gao
1,*
1
College of Animal Science & Technology, Yangzhou University, Yangzhou 225009, China
2
A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, Nakhimov av., 2, 299011 Sevastopol, Russia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Biology 2021, 10(10), 1005; https://doi.org/10.3390/biology10101005
Submission received: 30 August 2021 / Revised: 26 September 2021 / Accepted: 28 September 2021 / Published: 7 October 2021
(This article belongs to the Section Bioinformatics)
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Abstract

:

Simple Summary

Transposable elements, including DNA transposons, play a significant role in genetic material exchanges between prokaryotes and eukaryotes. Comparative profiling of the evolution pattern of DNA transposons between prokaryotes and eukaryotes may identify potential genetic material exchanges between them and provide insights into the evolutionary history of prokaryotic and eukaryotic genomes. The members of the IS630-Tc1-mariner (ITm) group may represent the most diverse and widely distributed DNA transposons in nature, and the discovery of new members of this group is highly expected based on the increasing availability of genome sequencing data. We discovered a new superfamily (termed Sailor) belonging to the ITm hyperfamily, which differed from the known superfamilies of Tc1/mariner, DDxD/pogo and DD34E/Gambol, regarding phylogenetic position and catalytic domain. Our data revealed that Sailor was distributed in both prokaryotes and eukaryotes and suggested that horizontal transfer (HT) events of Sailor may occur from prokaryotic to eukaryotic genomes. Finally, internal transmissions of Sailor in prokaryotes and eukaryotes were also detected.

Abstract

Here, a new superfamily of IS630-Tc1-mariner (ITm) DNA transposons, termed Sailor, is identified, that is characterized by a DD82E catalytic domain and is distinct from all previously known superfamilies of the ITm group. Phylogenetic analyses revealed that Sailor forms a monophyletic clade with a more intimate link to the clades of Tc1/mariner and DD34E/Gambol. Sailor was detected in both prokaryotes and eukaryotes and invaded a total of 256 species across six kingdoms. Sailor is present in nine species of bacteria, two species of plantae, four species of protozoa, 23 species of Chromista, 12 species of Fungi and 206 species of animals. Moreover, Sailor is extensively distributed in invertebrates (a total of 206 species from six phyla) but is absent in vertebrates. Sailor transposons are 1.38–6.98 kb in total length and encoded transposases of ~676 aa flanked by TIRs with lengths between 18, 1362 and 4 bp (TATA) target-site duplications. Furthermore, our analysis provided strong evidence of Sailor transmissions from prokaryotes to eukaryotes and internal transmissions in both. These data update the classification of the ITm group and will contribute to the understanding of the evolution of ITm transposons and that of their hosts.

1. Introduction

Transposable elements (TEs) are DNA sequences capable of integration and movement within the host genome. The proportion of TEs in the genomes of various organisms varies widely (from 3% to 90%) [1,2,3]. As a result of displacements, TEs can change the primary structure of DNA, interfere with the work of genes and change their function, influence the processes of regulation of transcription, and cause chromosomal rearrangements [4,5,6]. TE-mediated mutations are usually classified as insertional mutations [7,8]. Moreover, the epigenetic topology of the eukaryotic genome can change as a result of transpositions [9]. In addition, TE nucleotide sequences can be the source of new genes [10,11]. A large number of stress factors, both intracellular and external, have been shown to affect the induction of TE movements. These include high and low temperature, pH, ultraviolet radiation, magnetic fields, gamma radiation, various chemical compounds, outbreeding, inbreeding, infections, and starvation, among others [4]. A natural consequence of increased stress-induced mutagenesis is a growth in the spectrum of genetic diversity. In turn, this increases the adaptive potential of the population, which can also contribute to speciation [12,13]. Currently, TEs are divided into two classes: retrotransposons (class I) and DNA transposons (class II). Class I includes TEs that encode reverse transcriptase and are transported by an RNA intermediate, as well as their non-autonomous derivatives, whereas Class II combines TEs that use DNA to move their copies to a new position in the genome and can be divided into two subclasses. The first subclass consists of two groups of elements: TIR and Crypton. TIRs are characterized by terminal inverted repeats (TIRs) and the enzyme transposase, through which transposition occurs via a cut-and-paste mechanism. TIR transposons include the hAT, Merlin, Mutator, PiggyBac, PIF-Harbinger, IS630-Tc1-mariner and Transib TE groups, among others. Crypton elements use tyrosine recombinase in the transposition mechanism. Helitron and Maverick are the two main representative elements of the second subclass. These elements are moved using a copy-and-paste mechanism [5,11,14,15]. One of the most widespread groups of cut-and-paste DNA transposons is the IS630-Tc1-mariner (ITm). Members of this group are present in almost all branches of the tree of life [16]. Autonomous ITm transposons usually carry one open reading frame (ORF) encoding the transposase enzyme, flanked by TIRs. ITm transposases are characterized by the presence of a paired domain (two HTH motifs) and a DDE/D domain. In addition, structures such as the GRPR-type motif and a nuclear localization signal (NLS) are present [17,18]. The paired domain is in the first half of the amino acid sequence and provides specific binding to TIRs. The second half contains the DDE/D domain, which possesses the catalytic activity required for the excision and insertion of the TE. The GRPR-like motif is located between the two HTH motifs of the paired domain and is supposed to mediate the binding of the paired domain to the target site duplication (TSD), the TA dinucleotide [19], which has been identified in most Tc1/mariner superfamilies, such as DD35E/TR [20], DD36E/IC [21], DD38E/IT [22], DD37D/maT [23], DD39D/GT [23] and DD41D/VS [24]. The classification of ITm transposons is reliably associated with the length of the peptide chain between the second “D” and the third “E/D” amino acid residues (aa) of the catalytic domain, the so-called DDE/D signature. 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]. Consequently, the rank of the ITm group is automatically promoted to hyperfamily, because it includes more than one superfamily. This situation underscores the need to study new groups of ITm transposons and their prevalence among living organisms. Here, we identified a new superfamily of ITm, termed Sailor, that forms an independent superfamily with a distinct DDE domain (DD78-111E) and different phylogenetic positions compared with previous superfamilies (DDxD/pogo, DD34E/Gambol, Tc1/mariner, Zator and TP36) [25,26,30,31,32]. We also systematically characterized their evolution landscapes (taxonomic distribution and evolution patterns) and structural organization. The current study updated the classification of ITm DNA transposons and expanded our knowledge about the diversity of DNA transposons and their contributions to genome evolution in prokaryotes and eukaryotes.

2. Materials and Methods

2.1. Transposon Mining and Annotation

New transposon sequences were identified by systematically screening the new transposase families as part of the development of genetic manipulation tools using the TE database of RepBase. All Tc1/mariner DNA transposon sequences deposited in RepBase were downloaded (Version: 20181026). Transposase-coding sequences were predicted with GENSCAN (http://hollywood.mit.edu/GENSCAN.html, accessed on 15 October 2020). Subsequently, these transposases (>300 aa) were used for phylogenetic and multiple-alignment analyses, to define putative new families. The distinct DD82E domain of transposase was firstly identified in four species including Lobosporangium transversal (607 aa), Locusta migratoria (461 aa), Crassostrea gigas (376 aa), and Acyrthosiphon pisum (434 aa), which were deposited in RepBase. Then, these transposase sequences were used as a query to search the genomes deposited in the National Center for Biotechnology Information (NCBI) genome project database (https://blast.ncbi.nlm.nih.gov/Blast, accessed on 25 October 2020) using TBLASTN with an E-value of 1e–100. Subsequently, the best hits were extracted with 2-kb flanking sequences, since most ITm families contain TIRs (including untranslated region) less than 2 kb as previous studies reported, such as DD35E/TR [20], DD36E/IC [21], DD38E/IT [22], DD37D/maT [23], DD39D/GT [23]. The presence of TIRs and TSDs was manually screened in the resulting sequences, to identify potential DNA transposons. Putative sequence contamination was verified further by checking the flanking sequences of transposons, and the transposons located on very short contigs that failed to map to the species genome or lacked flanking sequences were designated as sequence contamination and were excluded from the analysis. The WebLogo server (http://weblogo.berkeley.edu/logo.cgi/, accessed on 10 April 2021) was used to create the logo representation of the TSD sequences [33]. Putative nuclear localization signal (NLS) motifs were predicted using PSORT II, as provided on the PSORT server (http://psort.nibb.ac.jp/, accessed on 25 April 2021), and the secondary structures and motifs of the transposases were predicted using the PSIPRED program (http://bioinf.cs.ucl.ac.uk/psipred/, accessed on 25 April 2021) [34], Pfam (http://pfam.xfam.org/, accessed on 26 April 2021) and HMMER web server (https://www.ebi.ac.uk/Tools/hmmer//search/phmmer, accessed on 28 April 2021). The consensus sequences of each transposon in each genome were reconstructed via the multiple alignment of copies in each genome using the online emboss explorer (http://www.bioinformatics.nl/emboss-explorer/, accessed on 5 April 2021). In cases where there were a few copies of the transposon in the genome, the longest copy in the genome was designated as the representative element for further analysis. The copy number of each transposon in each species was estimated based on the Blast result of the various genome sequences (>40% coverage in length and >80% identity) using consensus or representative sequences of the identified transposon as queries. All identified transposon sequences reported in this paper are deposited as Supplementary Material in FASTA format (Data S1).

2.2. Phylogenetic Analysis

The maximum likelihood method was used to infer the phylogenetic tree using the IQ-TREE program with an ultrafast bootstrap value of 1000, based on the alignment of the conserved DDE region of transposases [35]. The best-suited aa substitution model for these data was the LG+I+G4 model according to BIC, which was selected by ModelFinder embedded in the IQ-TREE program [35]. The MAFFT program was used to perform multiple alignments of DDE domains [36]. Reference transposase sequences were obtained from GenBank and the references of DD35E/TR [20], DD36E/IC [21], DD37E/TRT [27], DD38E/IT [22], Zator and TP36 [32]. Bacterial transposases from insertion sequence 256 (IS256) were chosen as the outgroup.

2.3. HT Detection

The pairwise distances between the host genes and the transposons were used to detect horizontal transfer events of Sailor transposons. In total, 29 ribosomal proteins (cytoplasmic and organelle) that were identified as universally conserved proteins [37] were evaluated for their conservation and length (Figures S1 and S2), as well as taxonomic distribution of the single genomic copy across domains (Table S1), to select the fit host genes for the HT hypothesis test. The accession numbers and host species are listed in Table S2. The taxonomic distribution of a single genomic copy of host genes across the domains of Bacteria, Archaea and Eucarya (Plantae, Chromista, Protozoa, Eumycota and animals) was evaluated using the online OrthoDB database (https://www.orthodb.org/, accessed on 5 May 2021). Homologous genes between prokaryote and eukaryote species were identified by an online TBlastN or BLASTP search using prokaryote proteins as queries. In addition, in order to obtain accurate results, only species containing intact transposons (full length elements coding transposase >300 aa flanked with TIRs) were selected for HT analysis. Putative HT events between organisms, as detected based on pairwise distances between the various organisms, were determined for Sailor and the selected host gene sequences using the MEGA program depending on two multiple alignments [38]. The multiple sequence alignments of the host-gene-coding sequences and transposase-coding sequences were created using the MAFFT program (version 7.481) [36]. Subsequently, comparison distances between the host genes and transposons were calculated using MEGA software (v. 7.0.26) based on two aligned files (pairwise deletion and maximum composite likelihood). Species for which we could not retrieve highly conserved host genes in the NCBI database were excluded from this analysis. The accession numbers and host species are listed in Table S3. The genetic distances between host genes and transposons in each species, as determined using a pairwise comparison, are listed in Tables S4 and S5.

3. Results

3.1. Discovery of a New Superfamily of ITm DNA Transposons, DD82E/Sailor

We identified a cluster of transposases with a new type of catalytic domain that was distinct from the known transposase superfamilies of the ITm group, most of which were represented by DD82E, but with variations between DD78E and DD111E (Figure 1, Table S6 and Data S2). The phylogenetic tree (Figure 2 and Figure S3), which was obtained via maximum likelihood method using the IQ-TREE program [35], demonstrated that DD82E/Sailor elements form a well-defined monophyletic clade with a high degree of support (99%). The Tc1/mariner transposons were the closest known group to DD82E/Sailor on the phylogenetic tree, which were grouped into a separate clade with 99% bootstrap support. Furthermore, the known superfamilies, including DD34E/Gambol [31], DDxD/pogo [30], Zator and TP36 [32], were identified, and formed separate clades with 100% bootstrap support. The listed groups formed branches separately with very high support (≥99%) for each clade and were “mixed” with IS630 transposons (Figure 2 and Figure S3), which is possibly related to the independent emergence of these groups from IS630 during evolution. Overall, the phylogenetic analysis showed that the discovered transposons of Sailor with a new type of catalytic domain (mainly represented by DD82E, with variation from DD78E to DD111E) are a new superfamily of the ITm infraclass, close to Tc1/mariner.

3.2. Distribution of DD82E/Sailor in Both Prokaryotes and Eukaryotes

According to Cavalier-Smith (1998) [39], the tree of life is subdivided into six kingdoms: Bacteria/Archaea, Chromista, Plantae, Protozoa, Fungi and Animals. Representatives of the new superfamily DD82E/Sailor were found in six kingdoms (Figure 3 and Table 1 and Table S6). For the species in which DD82E/Sailor was identified, the classification, structural characteristics, sequences and genome coordinates in each genome are listed in Table S6. Among Protozoa, only a few cases of the presence of DD82E/Sailor were identified: Amoebozoa (two species), Ichthyosporea (one species) and Choanoflagellatea (one species); in plantae, only two cases of the presence of DD82E/Sailor were identified: red algae (one species) and land plants (one species). The representation of the new transposons among Bacteria, Chromista (Stramenopiles) and Fungi was slightly higher; DD82E/Sailor transposons were found in nine, 23 and 12 species, respectively. The animal kingdom was much richer regarding the representation of DD82E/Sailor elements. Of note, although DD82E/Sailor transposons were common among invertebrates (206 species), including Porifera, Mollusca, Annelida, Nematoda, Arthropoda and Echinodermata, they were not found in vertebrates. A predominant proportion of elements of this superfamily was found in Protostomia (Mollusca (17 species), Annelida (one species), Nematoda (12 species) and Arthropoda (174 species)). In some species, DD82E/Sailor elements were found in the taxa Deuterostomia: Echinodermata (one species) and Porifera (one species). Among arthropods, DD82E/Sailor transposons were also not uniformly distributed; a clear predominance of their representation in insects was noted (Figure 3 and Table 1 and Table S6). Uniformity was also not observed within the class of insects, as the studied TEs were found only in 12 out of 29 taxa (Figure 3B). This mosaic distribution along the tree of life indicates a rich evolutionary history woven from elimination events and horizontal transpositions. The latter phenomenon is a fairly common feature of the ITm infraclass elements [40,41]. When counting the number of copies of the elements, only sequences with homology to more than 40% of the length of the representative copy and identity of more than 80% were considered. This analysis showed that the overall proliferation of Sailor was not significant (Table S6). In most cases, the number of copies ranged from a few to several dozen. However, in some representatives of Mollusca and Arthropoda, the number of copies of Sailor exceeded 100. The gastropod Mollusca Haliotis rubra (219) and representatives of the order Phasmatodea Arthropoda (83–341), in particular Timema cristinae (341), were especially rich in copies of Sailor. Furthermore, intact copies of Sailor were detected in four species in prokaryotes and in 55 species of 19 orders in eukaryotes, indicating recent insertion into the genome and that some elements may still be active in these species or lineages (Table S6).

3.3. Distinct Structural Organization of DD82E/Sailor

The structural organization of Sailor transposons retained the features of classic TIR TEs in all groups of organisms (Table S6). The structure of representative Sailor transposons is shown in Figure 4A and Figure S4. Full-size Sailor exhibited high variability in length (1379–6979 bp). Concomitantly, the elements of Bacteria were not very long (1379–1437 bp), whereas in some representatives of Stramenopiles, Porifera and Arthropoda, the length of Sailor exceeded 4 kb, and in Fungi it almost reached 7 kb (Table 1). In general, a length varying from 1.3 to 2.5 kb is typical of the representatives of the Tc1/mariner superfamily, whereas a length greater then 4 kb is more common among the DDxD/pogo superfamily [24,26,30]. Significant variations in the length of TIRs were also observed: “classic” TIRs (23–57 bp) were detected in most of the studied species, and extra-long TIRs (1362 bp) were found in Lobosporangium transversale (Fungi). The latter explains the colossal size of the TE itself (6979 bp). Very long TIRs were observed in representatives of DD41D/VS elements [24]. The first two nucleotides of Sailor TIRs are usually “GT” and “CC” di-nucleotides, and two conserved motifs (5–10 and 15–25 bp), which may be corresponding to the transposase recognition sequences, were identified for Sailor TIRs (Figure 4B). TSDs that predominantly shared Sailor contained four TATA nucleotides, in contrast to the classical TA dinucleotide present in Tc1/mariner elements (Figure 4C). Full-length Sailor elements had ORFs encoding transposases from amino acid residues 323 to 676. The longest amino acid sequences of the enzyme (over 500 amino acid residues) were detected in Stramenopiles, Arthropoda and Fungi (Table 1). In intact transposases, a DNA-binding domain, a catalytic domain and, in some cases, an NLS were observed (Figure 4A and Figure S4). The DNA-binding domain present in representatives of different taxa showed sufficient conservation. Concomitantly, although the catalytic domain had the DD82E signature in an overwhelming majority of cases, it exhibited high variability across taxa (DD78E-DD111E) (Figure 4D). The occurrence of a domain with the DD83E signature was also frequent (Stramenopiles, Mollusca, Annelida, Arthropoda and Echinodermata). Sailor transposases with the DD82E signature were not found among red algae, Fungi, Annelida, Nematoda and Echinodermata. Catalytic domains with a spacer between “D” and “E” of more than 90 amino acid residues were found in red algae, Stramenopiles, Nematoda and Arthropoda. Multiple alignment of the amino acid sequence of the catalytic domain of the Sailor elements together with DD34E/Tc1, DD35E/TR, DD36E/IC, DD37E/TRT and DD38E/IT showed that the increase in the length of the spacer between “D” and “E” was apparently caused by two insertion events of 13 and 36 aa (Figure 1). In addition, in the spacer located between “D” and “D”, an insert with a length of 12–15 aa was also detected. In Sailor transposons, the region upstream of “E” exhibited noticeable differences from the homologous region of Tc1 and Tc1-like elements, which may indicate a rather long-standing divergence, because this region is conserved in the Tc1/mariner superfamily. These insertion motifs were analyzed by the Pfam and HMMER web server, and we did not find any homology domain, and therefore their function remains unknown.

3.4. Evidence of HT Events of DD82E/Sailor between/within Prokaryotes and Eukaryotes

Pairwise genetic distance comparisons between the host genes and the transposons were used to identify putative horizontal transfer events of Sailor elements. Considering the deep phylogenetic relationships in prokaryotes and eukaryotes, the conservation, protein length and taxonomic distribution of the single genomic copy of 29 ribosomal proteins, designated as the universally conserved genes [37], were evaluated to select the fit host genes for genetic distance calculation in the HT hypothesis test. An analysis of these data suggested that the L3 and L4 ribosomal proteins (cytoplasmic and organelle), which display higher sequence identities and are greater in length (Figures S1 and S2), and a wider taxonomic distribution of the single genomic copy across the three domains of Bacteria, Archaea and Eucarya (Table S1) were fit for the estimation of genetic distance between species as the host genes. The accession numbers and host species are listed in Table S2. The taxonomic distribution of the single genomic copy of the host gene across domains, which was evaluated using the online OrthoDB database (https://www.orthodb.org/, accessed on 5 May 2021), was compared and applied to minimize gene duplication in genomes, for improving the accuracy of genetic distance estimation between species. The genes that were homologous between prokaryote and eukaryote species were identified via online TBlastN or BLASTP search using the prokaryotic ribosomal L3 and L4 proteins as queries; all prokaryote L3 and L4 ribosomal proteins hit eukaryote organelle L3 and L4 ribosomal proteins, respectively. Thus, the prokaryote L3 and L4 ribosomal proteins were compared with eukaryote organelle L3 and L4 ribosomal proteins, to calculate the genetic distance of host genes between prokaryote and eukaryote species, whereas cytoplasmic L3 and L4 ribosomal proteins were used for the calculation of the genetic distance of host genes between eukaryote species. HT was considered to occur when the genetic distances of transposons were lower than those of both L3 and L4 host genes between species. Based on the pairwise genetic distance comparisons, overall, HT events were supported by more than 110 species pairs (Figure 5 and Figure S5 and Table S7), HTs from prokaryotes (four species) to eukaryotes (43 species) were supported by 103 species pairs: most HT events (98 species pairs) were identified between bacteria (four species) and Arthropoda (41 species), HTs between Deltaproteobacteria and arthropods were supported by 77 species pairs, HTs between Gammaproteobacteria and arthropods were supported by 21 species pairs, HT between bacteria and Nematoda, and HT between bacteria and Mollusca were supported by one and four species pairs, respectively (Figure 5A,D and Tables S4 and S7). HT events were also detected between species within prokaryotes (six species pairs), HT events between Gammaproteobacteria and Deltaproteobacteria were supported by three species pairs, HT events within Deltaproteobacteria were supported by three species pairs as well (Figure 5B,D and Tables S5 and S7). In addition, HT events of Sailor were detected between eukaryotic species (Figure 5C,D and Tables S5 and S7), including HT between species of Nematoda (one species pair) and HT between species of Arthropoda (four species pairs).

4. Discussion

4.1. Extensive Distribution of Sailor

The DNA transposons with the DD82E signature described in this work represent a new superfamily of transposons, which we called Sailor (Figure 2 and Table S6). This superfamily was phylogenetically closest to the Tc1/mariner superfamily and was part of a large group (infraclass) of DNA transposons known as IS630-Tc1-mariner (ITm) [26,29,30]. Representatives of the Tc1/mariner superfamily and the DD34E/Gambol and DDxD/pogo superfamilies (also referred to as ITm transposons) are found only in eukaryotes, whereas representatives of Sailor were identified among both eukaryotes and prokaryotes, across the six natural kingdoms (Figure 3). Despite the wide coverage of natural kingdoms, the taxon distribution of Sailor was highly mosaic compared with that of Tc1/mariner and DDxD/pogo. In total, Sailor elements were identified in 256 species (Table S6). Concomitantly, intact copies were detected only in a quarter of organisms (four prokaryotes and 55 eukaryotes). The counting of the number of copies showed a rather weak amplification (with few exceptions) of Sailor elements. Nevertheless, there were species in which more than 50 intact copies were identified in the genome. These were representatives of the order Coleoptera (Insecta; Anoplophora glabripennis and Callosobruchus maculatus) (Table S6). A large number of intact copies may indicate that the life cycle of these TEs is undergoing an amplification stage or has recently completed it. The TE life cycle includes the stages of invasion, amplification, diversification, inactivation (degradation) and elimination [43]. However, the life cycle may not always be complete. Variants are possible when TEs are immobilized and cannot proceed to the amplification stage or are weakly amplified and degrade relatively quickly. In addition, TE “resurrection” options are possible: horizontal transfer or intragenomic life-cycle restart [23,44]. Moreover, it is also possible to avoid “death” via the transition from the “wild” to “domestication” state, i.e., co-optation of the TE gene by the host genome [10,45].

4.2. Structural Organization of Sailor

The Tc1/mariner transposons were closest to the Sailor transposons on the phylogenetic tree (Figure 2). The study of the structural organization of Sailor elements allowed us to highlight several obvious differences from the representatives of the Tc1/mariner superfamily (Figure 1 and Figure 4). The most striking difference was undoubtedly the DDE signature. Tc1/mariner elements are characterized by the presence of the DD34-41E/D signature [20,21,22,23,24,27,28,29,30]. Although the Sailor superfamily was shown to contain the DD82E catalytic domain, this characteristic varied widely across Sailor members (DD78-111E) (Figure 4C). Concomitantly, the occurrence of the DD83E signature was also quite frequent, and the DD82E signature was not found among some taxa. Presumably, the lengthening of the catalytic domain occurred as a result of two independent insertions into the spacer located between “D” and “E” (Figure 1). Increasing the length of the spacer between “D” and “E” did not stop Sailor elements from spreading through the tree of life. Moreover, this spread did not reach a wide scale (Figure 3 and Table 1). Another important difference between Sailor and Tc1/mariner transposons was the TSD modification. Elements of the Tc1/mariner superfamily and members of the entire ITm infraclass recognize the TA dinucleotide and duplicate it as a result of insertion. This process provides an AT-hook (GRPR-motif) located in the transposase between the first and second triad of α-helices of the DNA-binding domain [19]. The TSDs in the majority of Sailor elements had four TATA nucleotides (Figure 4B). It is likely that, in the Sailor transposases, the motif that provides the connection with the TSD has also undergone changes. This change in the specificity of the insertion could have influenced the proliferation of Sailor transposons, as the number of potential insertion sites was significantly reduced. There were noticeable differences in the amino acid sequence of the conservative loci of the catalytic domain of transposases. For example, the region located around the first “D” in Sailor was I/VVYLDET, the consensus amino acid sequence around the second “D” was VIIMDNA, and the consensus sequence around the “E” was HCELNPIEL (Figure 1). By contrast, in Tc1/mariner, the corresponding loci are VLWSDES, IFQQDNA/D and SPDLNPIEN. The total length, the length of TIRs and the length of the transposase of Sailor elements exhibited a fairly high variability (Table 1); however, this phenomenon is often observed in different groups of the ITm infraclass [20,21,22,23,24,27,28,29,30]. The totality of all of these established differences in structural organization suggests that Sailor transposons have passed a long independent evolutionary path. In combination with the data of the phylogenetic analysis and the identified cases of HT, it is most likely that Sailor, as a separate evolutionary group, was formed in prokaryotes and then spread along the tree of life as a result of HT.

4.3. HT Events of DD82E/Sailor between/within Prokaryotes and Eukaryotes

Although a large number of cases of prokaryote-to-eukaryote gene HTs have been identified [46,47,48,49], and prokaryote-to-prokaryote [50] and eukaryote-to-eukaryote cases of TE HT have been reported extensively [20,21,22,51,52,53,54], very few TEs are known to have jumped from prokaryotes to eukaryotes. One likely such event has been reported, in which several bacterial TEs were found embedded in larger genomic fragments that were transferred horizontally from bacteria to eukaryotes [55]. In another study, typical prokaryote-to-eukaryote HT of TEs were characterized, although they occurred at relatively low frequency [47]. The current study revealed that Sailor elements are apparently characterized by a high frequency of cases of horizontal transfer from prokaryotes to eukaryotes. In total, HTs were supported by more than 110 species pairs based on the genetic distance comparisons between transposons and the two host genes. HT from prokaryotes to eukaryotes were supported by over 100 species pairs (Figure 5A), and most HT events occurred between bacteria and invertebrate (Arthropoda) species. Whereas, a low frequency of HT was observed within eukaryotes, which may also explain why Sailor transposons are more common in invertebrates, but absent in vertebrates. The Tc1/mariner superfamily is the record holder among TEs for established HT cases [40,41]. It is likely that Sailor, as part of the ITm Infraclass, inherited the ability of undergoing frequent HT. Since the discovery of HT, many articles have been published describing this phenomenon in various taxa of eukaryotes (plants, insects, reptiles, mammals and others). It has been shown that these events can occur both between closely related species and distant taxa [40,54,56,57,58,59,60]. To date, about 3000 HT events have been described, with about a third of them being associated with elements of the Tc1/mariner superfamily [41]. Despite the abundance of literature on and the high number of detected cases of HT transposons, the mechanism underlying this phenomenon remains unclear. Questions about the probability of generation of adaptive insertions into the recipient’s genome and about their contribution to the evolution of genomes and speciation also remain open. However, the identification of new cases of HT will help expand our knowledge of this phenomenon and bring us closer to solving the issues discussed above. The identification of HT cases between prokaryotes and eukaryotes demonstrates the possibility of exchange of genetic information between two different domains of life. In addition, in the current study, the HT events tended to be underestimated because we applied universally conserved genes, and some host gene annotations were not available. Furthermore, we only used the intact transposons to perform the HT test for accuracy. Thus, we did not define the number of independent HT events of Sailor in this report. The lower number of HTs of Sailor observed in arthropoda using the pairwise genetic distance comparisons based on L3 and transposon compared with those of L4 and transposon was attributed to the lower number of L3 proteins (only three species) vs. L4 proteins (seven species) annotated in this lineage.

5. Conclusions

A superfamily (DD82E/Sailor) of ITm transposons was discovered in this study that displayed a distinct structural organization and phylogenetic position compared with the known groups of ITm, including Tc1/mariner, DDxD/pogo and DD34E/Gambol. Moreover, they were distributed in both prokaryotic and eukaryotic organisms, and HT events of these elements may have occurred from prokaryotic to eukaryotic organisms and between different kingdoms. This observation not only improves our understanding of the evolution of the Sailor superfamily, but also expands our understanding of the diversity of ITm transposons and updates the classification of this group.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/biology10101005/s1, Figure S1. Sequence identity of 29 universally conserved ribosomal proteins. (A) Organelle ribosomal proteins, (B) cytoplasmic ribosomal proteins. The original data are listed in Table S8. Figure S2. Sequence length of 29 universally conserved ribosomal proteins. (A) Organelle ribosomal proteins, (B) cytoplasmic ribosomal proteins. The original data are listed in Table S9. Figure S3. Uncollapsed phylogenetic position of the Sailor superfamily. Figure S4. Motif prediction for Sailor transposases. This analysis was performed using multiple alignment with Bioedit and with modifications in Genedoc. The green box represents the range of the α-helix of all sequences; the red box represents the range of DDE sequences; the red font represents the NLS sequence. (Sailor-Delbac: Deltaproteobacteria bacterium; Sailor-Pytoli: Pythium oligandrum; Sailor-Lobtra: Lobosporangium transversal; Sailor-Halrub: Haliotis rubra; Sailor-Hydele: Hydroides elegans; Sailor-Caenig: Caenorhabditis nigoni; Sailor-Calmac: Callosobruchus maculatus; Sailor-Timcri: Timema cristinae) Figure S5. HT events of Sailor. (A) The distances were obtained from all possible pairwise comparisons L3 (cytoplasm ribosomal protein L3 in Prokaryotic and organelles ribosomal protein L3 in eukaryotic) and Sailor. (B)The distances were obtained from all possible pairwise comparisons L4 (cytoplasm ribosomal protein L4 in Prokaryotic and cytoplasm ribosomal protein L4 in eukaryotic) and Sailor. (C) The distances were obtained from all possible pairwise comparisons L3 (cytoplasm ribosomal protein L3) and Sailor. (D) The distances were obtained from all possible pairwise comparisons L4 (cytoplasm ribosomal protein L4) and Sailor. (E) The distances were obtained from all possible pairwise comparisons L3 (cytoplasm ribosomal protein L3) and Sailor. (F) The distances were obtained from all possible pairwise comparisons L4 (cytoplasm ribosomal protein L4) and Sailor. Table S1. Number of single copy species, species and genes of 29 universally conserved ribosomal proteins. Table S2. Accession numbers of 29 generally conserved ribosomal proteins. Table S3. Accession numbers of ribosomal proteins of species involved in horizontal transmission. Table S4. Distance between Sailor and host genes (from prokaryotic to eukaryotic organisms). Table S5. Distance between Sailor and host genes (in prokaryotes and eukaryotes). Table S6. Details of Sailor, including species distribution, protein length, TIR, etc. Table S7. HT event statistics of Sailor. Table S8. The sequence identity statistics of 29 universally conserved ribosomal proteins. Table S9. The sequence length statistics of 29 universally conserved ribosomal proteins. Data S1. Sailor transposons. Data S2. Multiple alignment of catalytic domains including reference families of DD34E/Gambol, DD34E/Tc1, DD35E/TR, DD36E/IC, DD37E/TRT, and DD38E/IT. Data S3. Multiple alignments of the organelle ribosomal protein L3. Data S4. Multiple alignments of the organelle ribosomal protein L4. Data S5. Multiple alignments of the cytoplasmic ribosomal protein L3. Data S6. Multiple alignments of the cytoplasmic ribosomal protein L4. Data S7. Multiple alignment of Sailor (organelle ribosomal protein L3). Data S8. Multiple alignment of Sailor (organelle ribosomal protein L4). Data S9. Multiple alignment of Sailor (cytoplasmic ribosomal protein L3). Data S10. Multiple alignment of Sailor (cytoplasmic ribosomal protein L4).

Author Contributions

B.G. and C.S. conceived and designed the study. S.S., Z.G., M.P., K.X., M.D., Y.W. and S.W. mined transposons, collected data and performed the data analysis. M.P., S.S. and C.S. wrote the manuscript. All have authors read and approved the final version of the manuscript.

Funding

This research was funded by grants from the National Genetically Modified Organisms Breeding Major Projects program (2018ZX08010-08B), Russian Academy of Sciences (121041400077-1), the National Natural Science Foundation of China (31671313), the Priority Academic Program Development of Jiangsu Higher Education Institutions, and the High-end Talent Support Program of Yangzhou University to Chengyi Song.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank Cai Chen and Naisu Yang for their advice on transposon mining and data analysis.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kidwell, M.G. Transposable elements and the evolution of genome size in eukaryotes. Genetica 2002, 115, 49–63. [Google Scholar] [CrossRef] [PubMed]
  2. Guo, B.C.; Zou, M.; Gan, X.N.; He, S.P. Genome size evolution in pufferfish: An insight from BAC clone-based Diodon holocanthus genome sequencing. BMC Genom. 2010, 11, 396. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. de Koning, A.P.J.; Gu, W.; Castoe, T.A.; Batzer, M.A.; Pollock, D.D. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 2011, 7, e1002384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Yurchenko, N.N.; Kovalenko, L.V.; Zakharov, I.K. Transposable elements: Instability of genes and genomes. Russ. J. Genet. Appl. Res. 2011, 1, 489–496. [Google Scholar] [CrossRef]
  5. Grabundzija, I.; Messing, S.A.; Thomas, J.; Cosby, R.L.; Bilic, I.; Miskey, C.; Döring, A.G.; Kapitonov, V.; Diem, T.; Dalda, A.; et al. A Helitron transposon reconstructed from bats reveals a novel mechanism of genome shuffling in eukaryotes. Nat. Commun. 2016, 7, 10716. [Google Scholar] [CrossRef] [Green Version]
  6. Chandler, M.; Gellert, M.; Lambowitz, A.M.; Rice, P.A.; Sandmeyer, S.B. Mobile DNA III; ASM Press: Washington, DC, USA, 2015. [Google Scholar]
  7. Levin, H.L.; Moran, J.V. Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 2011, 12, 615–627. [Google Scholar] [CrossRef]
  8. Sturm, Á.; Perczel, A.; Ivics, Z.; Vellai, T. The Piwi-piRNA pathway: Road to immortality. Aging Cell 2017, 16, 906–911. [Google Scholar] [CrossRef]
  9. Fedoroff, N.V. Transposable Elements, Epigenetics, and Genome Evolution. Science (New York N. Y.) 2012, 338, 758–767. [Google Scholar] [CrossRef] [Green Version]
  10. Sinzelle, L.; Izsvák, Z.; Ivics, Z. Molecular domestication of transposable elements: From detrimental parasites to useful host genes. Cell. Mol. Life Sci. 2009, 66, 1073–1093. [Google Scholar] [CrossRef]
  11. Bourque, G.; Burns, K.H.; Gehring, M.; Gorbunova, V.; Seluanov, A.; Hammell, M.; Imbeault, M.; Izsvák, Z.; Levin, H.L.; Macfarlan, T.S.; et al. Ten things you should know about transposable elements. Genome Biol. 2018, 19, 199. [Google Scholar] [CrossRef]
  12. Piacentini, L.; Fanti, L.; Specchia, V.; Bozzetti, M.P.; Berloco, M.; Palumbo, G.; Pimpinelli, S. Transposons, environmental changes, and heritable induced phenotypic variability. Chromosoma 2014, 123, 345–354. [Google Scholar] [CrossRef] [Green Version]
  13. Auvinet, J.; Graça, P.; Belkadi, L.; Petit, L.; Bonnivard, E.; Dettaï, A.; Detrich, W.H.; Costaz, C.O.; Higuet, D. Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: The case for the Antarctic teleost genus Trematomus. BMC Genom. 2018, 19, 339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Wicker, T.; Sabot, F.; Van, A.H.; Bennetzen, J.L.; Capy, P.; Chalhoub, B.; Flavell, A.; Leroy, P.; Morgante, M.; Panaud, O.; et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 2007, 8, 973–982. [Google Scholar] [CrossRef]
  15. Kojima, K.K. Structural and sequence diversity of eukaryotic transposable elements. Genes Genet. Syst. 2018, 94, 233–252. [Google Scholar] [CrossRef] [Green Version]
  16. Yuan, Y.W.; Wessler, S.R. The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc. Natl. Acad. Sci. USA 2011, 108, 7884–7889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Ivics, Z.; Hackett, P.B.; Plasterk, R.H.; Izsvák, Z. Molecular Reconstruction of Sleeping Beauty, a Tc1-like Transposon from Fish, and Its Transposition in Human Cells. Cell 1997, 91, 501–510. [Google Scholar] [CrossRef] [Green Version]
  18. Plasterk, R.H.A.; Izsvák, Z.; Ivics, Z. Resident aliens: The Tc1/mariner superfamily of transposable elements. Trends Genet. 1999, 15, 326. [Google Scholar] [CrossRef]
  19. Zoltán, I.; Zsuzsanna, I. Sleeping Beauty Transposition. Microbiol. Spectr. 2015, 3, 2. [Google Scholar]
  20. Zong, W.C.; Gao, B.; Diaby, M.; Shen, D.; Wang, S.S.; Wang, Y.L.; Sang, Y.T.; Chen, C.; Wang, X.Y.; Song, C.Y. Traveler, a New DD35E Family of Tc1/Mariner Transposons, Invaded Vertebrates Very Recently. Genome Biol. Evol. 2020, 12, 66–76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  21. Sang, Y.T.; Gao, B.; Diaby, M.; Zong, W.C.; Chen, C.; Shen, D.; Wang, S.S.; Wang, Y.L.; Ivics, Z.; Song, C.Y. Incomer, a DD36E family of Tc1/mariner transposons newly discovered in animals. Mob. DNA 2019, 10, 45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Gao, B.; Zong, W.C.; Miskey, C.; Ullah, N.; Diaby, M.; Chen, C.; Wang, X.Y.; Ivics, Z.; Song, C.Y. Intruder (DD38E), a recently evolved sibling family of DD34E/Tc1 transposons in animals. Mob. DNA 2020, 11, 32. [Google Scholar] [CrossRef] [PubMed]
  23. Wang, S.; Diabya, M.; Puzakov, M.; Ullaha, N.; Wang, Y.l.; Danley, P.; Chen, C.; YanWang, X.; Gao, B.; Song, C.Y. Divergent evolution profiles of DD37D and DD39D families of Tc1/mariner transposons in eukaryotes. Mol. Phylogenetics Evol. 2021, 107143. [Google Scholar] [CrossRef] [PubMed]
  24. Shen, D.; Gao, B.; Miskey, C.; Chen, C.; Sang, Y.T.; Zong, W.C.; Wang, S.S.; Wang, Y.L.; Wang, X.Y.; Ivics, Z.; et al. Multiple Invasions of Visitor, a DD41D Family of Tc1/mariner Transposons, throughout the Evolution of Vertebrates. Genome Biol. Evol. 2020, 12, 1060–1073. [Google Scholar] [CrossRef] [PubMed]
  25. Shao, H.G.; Tu, Z.J. Expanding the diversity of the IS630-Tc1-mariner superfamily: Discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 2001, 159, 1103–1115. [Google Scholar] [CrossRef] [PubMed]
  26. Tellier, M.; Bouuaert, C.C.; Chalmers, R. Mariner and the ITm Superfamily of Transposons. Microbiol. Spectr. 2014, 3, MDNA3-0033-2014. [Google Scholar]
  27. Zhan, H.H.; Li, G.Y.; Xiong, X.M.; Ha, M.J.; Dai, F.Y. TRT, a Vertebrate and Protozoan Tc1-Like Transposon: Current Activity and Horizontal Transfer. Genome Biol. Evol. 2016, 8, 2994–3005. [Google Scholar] [CrossRef] [Green Version]
  28. Puzakov, M.; Puzakova, L.V.; Cheresiz, S.V. The Tc1-like elements with the spliceosomal introns in mollusk genomes. Mol. Genet. Genom. 2020, 295, 621–633. [Google Scholar] [CrossRef]
  29. Dupeyron, M.; Baril, T.; Bass, C.; Hayward, A. Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements. Mob. DNA 2020, 11, 21. [Google Scholar] [CrossRef]
  30. Gao, B.; Wang, Y.L.; Diaby, M.; Zong, W.C.; Shen, D.; Wang, S.; Chen, C.; Wang, X.; Song, C. Evolution of pogo, a separate superfamily of IS630-Tc1-mariner transposons, revealing recurrent domestication events in vertebrates. Mob. DNA 2020, 11, 25. [Google Scholar] [CrossRef]
  31. Coy, M.R.; Tu, Z.J. Gambol and Tc1 are two distinct families of DD34E transposons: Analysis of the Anopheles gambiae genome expands the diversity of the IS630-Tc1-mariner superfamily. Insect Mol. Biol. 2010, 14, 537–546. [Google Scholar] [CrossRef]
  32. Bao, W.; Jurka, M.G.; Kapitonov, V.V.; Jurka, J. New Superfamilies of Eukaryotic DNA Transposons and Their Internal Divisions. Mol. Biol. Evol. 2009, 26, 983–993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Crooks, G.E.; Hon, G.; Chandonia, J.M.; Brenner, S.E. WebLogo: A Sequence Logo Generator. Genome Res. 2004, 14, 1188–1190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. McGuffin, L.J.; Bryson, K. The PSIPRED protein structure prediction server. Bioinformatics 2000, 16, 404–405. [Google Scholar] [CrossRef] [PubMed]
  35. Nguyen, L.T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef] [PubMed]
  36. Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772. [Google Scholar] [CrossRef] [Green Version]
  37. Harris, J.K.; Kelley, S.T.; Spiegelman, G.B.; Pace, N.R. The genetic core of the universal ancestor. Genome Res. 2003, 13, 407–412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Sudhir, K.; Glen, S.; Koichiro, T. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870. [Google Scholar]
  39. Smith, T.C. A revised six-kingdom system of life. Biol. Rev. Camb. Philos. Soc. 1998, 73, 203–266. [Google Scholar] [CrossRef]
  40. Dupeyron, M.; Leclercq, S.; Cerveau, N.; Bouchon, D.; Gilbert, C. Horizontal transfer of transposons between and within crustaceans and insects. Mob. DNA 2014, 5, 4. [Google Scholar] [CrossRef] [Green Version]
  41. Wallau, G.L.; Vieira, C.; Loreto, É.L.S. Genetic exchange in eukaryotes through horizontal transfer: Connected by the mobilome. Mob. Dna 2018, 9, 6. [Google Scholar] [CrossRef]
  42. Hedges, S.B.; Marin, J.; Suleski, M.; Paymer, M.; Kumar, S. Tree of Life Reveals Clock-Like Speciation and Diversification. Mol. Biol. Evol. 2015, 32, 835–845. [Google Scholar] [CrossRef] [PubMed]
  43. Schaack, S.; Gilbert, C.; Feschotte, C. Promiscuous DNA: Horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol. Evol. 2010, 25, 537–546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Blumenstiel, J.P. Birth, School, Work, Death, and Resurrection: The Life Stages and Dynamics of Transposable Element Proliferation. Genes 2019, 10, 335. [Google Scholar] [CrossRef] [Green Version]
  45. Jangam, D.; Feschotte, C.; Betrán, E. Transposable Element Domestication As an Adaptation to Evolutionary Conflicts. Trends Genet. 2017, 33, 817–831. [Google Scholar] [CrossRef] [PubMed]
  46. Keeling, P.J.; Palmer, J.D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 2008, 9, 605–618. [Google Scholar] [CrossRef] [PubMed]
  47. Gilbert, C.; Cordaux, R. Horizontal Transfer and Evolution of Prokaryote Transposable Elements in Eukaryotes. Genome Biol. Evol. 2013, 5, 822–832. [Google Scholar] [CrossRef] [Green Version]
  48. Hall, R.J.; Whelan, F.J.; McInerney, J.; Ou, Y.Q.; Sananes, M.R.D. Horizontal Gene Transfer as a Source of Conflict and Cooperation in Prokaryotes. Front. Microbiol. 2020, 11, 1569. [Google Scholar] [CrossRef]
  49. Gilbert, C.; Schaack, S.; Pace, J.K., II; Brindley, J.P.; Feschotte, C. A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 2010, 464, 1347. [Google Scholar] [CrossRef] [Green Version]
  50. Touchon, M.; Rocha, E.P.C. Causes of Insertion Sequences Abundance in Prokaryotic Genomes. Mol. Biol. Evol. 2007, 24, 969–981. [Google Scholar] [CrossRef] [Green Version]
  51. Zhang, H.H.; Cédric, F.; Han, M.J.; Zhang, Z. Recurrent Horizontal Transfers of Chapaev Transposons in Diverse Invertebrate and Vertebrate Animals. Genome Biol. Evol. 2014, 6, 1375–1386. [Google Scholar] [CrossRef] [Green Version]
  52. Walsh, A.M.; Kortschak, R.D.; Gardner, M.G.; Bertozzi, T.; Adelson, D.L. Widespread horizontal transfer of retrotransposons. Proc. Natl. Acad. Sci. USA 2012, 110, 1012–1016. [Google Scholar] [CrossRef] [Green Version]
  53. Wallau, G.L.; Ortiz, M.F.; Loreto, E.L.S. Horizontal Transposon Transfer in Eukarya: Detection, Bias, and Perspectives. Genome Biol. Evol. 2012, 4, 801–811. [Google Scholar] [CrossRef] [Green Version]
  54. Tang, Z.; Zhang, H.H.; Huang, K.; Zhang, X.G.; Han, M.J.; Zhang, Z. Repeated horizontal transfers of four DNA transposons in invertebrates and bats. Mob. DNA 2015, 6, 3. [Google Scholar] [CrossRef] [Green Version]
  55. Dunning, H.J.C. Horizontal gene transfer between bacteria and animals. Trends Genet. 2011, 27, 157–163. [Google Scholar] [CrossRef] [Green Version]
  56. Novick, P.; Smith, J.; Ray, D.; Boissinot, S. Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. Gene 2010, 449, 85–94. [Google Scholar] [CrossRef]
  57. Gilbert, C.; Hernandez, S.S.; Flores-Benabib, J.; Smith, E.N.; Feschotte, C. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol. Biol. Evol. 2012, 29, 503–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Oliveira, S.G.; Bao, W.; Martins, C.; Jurka, J. Horizontal transfers of Mariner transposons between mammals and insects. Mob. DNA 2012, 3, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Lin, X.; Faridi, N.; Casola, C. An Ancient Transkingdom Horizontal Transfer of Penelope-Like Retroelements from Arthropods to Conifers. Genome Biol. Evol. 2016, 8, 1252–1266. [Google Scholar] [PubMed] [Green Version]
  60. Suh, A.; Witt, C.C.; Menger, J.; Sadanandan, K.R.; Podsiadlowski, L.; Gerth, M.; Weigert, A.; McGuire, J.A.; Mudge, J.; Edwards, S.V.; et al. Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes. Nat. Commun. 2016, 7, 11396. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. Schematic diagram of the catalytic domains of transposases, which include DD82E/Sailor, DD34E/Gambol, DD34E/Tc1, DD35E/TR, DD36E/IC, DD37E/TRT and DD38E/IT.
Figure 1. Schematic diagram of the catalytic domains of transposases, which include DD82E/Sailor, DD34E/Gambol, DD34E/Tc1, DD35E/TR, DD36E/IC, DD37E/TRT and DD38E/IT.
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Figure 2. Phylogenetic position of the Sailor superfamily. This phylogenetic tree was generated based on DDE domains using the maximum likelihood method in the IQ-TREE program with an ultrafast bootstrap approach (1000 replicates). The reference families and elements included DD34E/Tc1, DD34E/Gambol, DD35E/TR, DD36E/IC, DD37E/TRT, DD38E/IT, DD34D/mariner, DD37D/maT, DD39D/GT, DD41D/VS, DDxD/pogo, IS630 transposases, TP36, and Zator. IS256 was used as an outgroup. The uncollapsed tree is presented in Figure S3.
Figure 2. Phylogenetic position of the Sailor superfamily. This phylogenetic tree was generated based on DDE domains using the maximum likelihood method in the IQ-TREE program with an ultrafast bootstrap approach (1000 replicates). The reference families and elements included DD34E/Tc1, DD34E/Gambol, DD35E/TR, DD36E/IC, DD37E/TRT, DD38E/IT, DD34D/mariner, DD37D/maT, DD39D/GT, DD41D/VS, DDxD/pogo, IS630 transposases, TP36, and Zator. IS256 was used as an outgroup. The uncollapsed tree is presented in Figure S3.
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Figure 3. Taxonomic distribution of Sailor. (A) Taxonomic distribution of Sailor elements in the different kingdoms. The numbers next to the animal silhouettes represent the number of Sailor elements detected in the species of each lineage. The number after the slash represents the intact Sailor. (B) Taxonomic distribution of Sailor elements in Insecta. The taxonomic tree represents the distribution of the species identified in Insecta in their respective orders. Insecta orders are labelled with a square node and the number of Insecta species is shown outside the circle. The phylogenetic relationships were taken from the TimeTree database (http://timetree.org/, accessed on 5 June 2021) [42].
Figure 3. Taxonomic distribution of Sailor. (A) Taxonomic distribution of Sailor elements in the different kingdoms. The numbers next to the animal silhouettes represent the number of Sailor elements detected in the species of each lineage. The number after the slash represents the intact Sailor. (B) Taxonomic distribution of Sailor elements in Insecta. The taxonomic tree represents the distribution of the species identified in Insecta in their respective orders. Insecta orders are labelled with a square node and the number of Insecta species is shown outside the circle. The phylogenetic relationships were taken from the TimeTree database (http://timetree.org/, accessed on 5 June 2021) [42].
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Figure 4. Schematic representation of the structure of Sailor transposons. (A) Structural organization of Sailor elements. The yellow arrows represent Sailor, the black rectangles represent HTH motifs, the yellow circle represents the NLS, the pink rectangles represent the catalytic domains, and the blue regions represent transposases (Sailor-Delbac (Deltaproteobacteria bacterium), Sailor-Phyoil (Pythium oligandrum), Sailor-Lobtra (Lobosporangium transversale), Sailor-Halrub (Haliotis rubra), Sailor-Hydele (Hydroides elegans), Sailor-Caenig (Caenorhabditis nigoni), Sailor-Calmac (Callosobruchus maculatus), Sailor-Timcri (Timema cristinae)). (B) The WebLogo server (http://weblogo.berkeley.edu/logo.cgi/, accessed on 15 September 2021) was used to create the logo representation of the TIR (≤45 bp) sequences. The value 2 (log2 4) on the y axis stands for maximum possible frequency. (C) The WebLogo server (http://weblogo.berkeley.edu/logo.cgi/, accessed on 25 April 2021) was used to create the logo representation of the TSD sequences. (D) The table shows the situation of different kingdoms of DDxE, with the number placed after the slash representing the number of DDxE.
Figure 4. Schematic representation of the structure of Sailor transposons. (A) Structural organization of Sailor elements. The yellow arrows represent Sailor, the black rectangles represent HTH motifs, the yellow circle represents the NLS, the pink rectangles represent the catalytic domains, and the blue regions represent transposases (Sailor-Delbac (Deltaproteobacteria bacterium), Sailor-Phyoil (Pythium oligandrum), Sailor-Lobtra (Lobosporangium transversale), Sailor-Halrub (Haliotis rubra), Sailor-Hydele (Hydroides elegans), Sailor-Caenig (Caenorhabditis nigoni), Sailor-Calmac (Callosobruchus maculatus), Sailor-Timcri (Timema cristinae)). (B) The WebLogo server (http://weblogo.berkeley.edu/logo.cgi/, accessed on 15 September 2021) was used to create the logo representation of the TIR (≤45 bp) sequences. The value 2 (log2 4) on the y axis stands for maximum possible frequency. (C) The WebLogo server (http://weblogo.berkeley.edu/logo.cgi/, accessed on 25 April 2021) was used to create the logo representation of the TSD sequences. (D) The table shows the situation of different kingdoms of DDxE, with the number placed after the slash representing the number of DDxE.
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Figure 5. HT events of Sailor. (A) The two organelle ribosomal proteins (L3 and L4) exhibited prokaryotic to eukaryotic HT events. The yellow color represents the HT characteristic of the organelle ribosomal protein L3, the dark-green color represents HT common to the organelle ribosomal proteins L3 and L4, and the light-green color represents the HT characteristic of the organelle ribosomal protein L4. (B) The two cytoplasmic ribosomal proteins (L3 and L4) exhibited HT events in prokaryotic species. The dark-green color represents HT common to the cytoplasmic ribosomal proteins L3 and L4. (C) The two cytoplasmic ribosomal proteins (L3 and L4) exhibited HT events in eukaryotic species. The yellow color represents the HT characteristic of the cytoplasm ribosomal protein L3, the dark-green color represents HT common to the cytoplasmic ribosomal proteins L3 and L4, and the light-green color represents the HT characteristic of the cytoplasm ribosomal protein L4. (D) HT based on the pairwise genetic distance comparisons of two proteins. The numbers next to the animal silhouettes represent species pairs supporting HT events in the same phylum, and the numbers behind the curve represent species pairs supporting HT events from prokaryotic to eukaryotic species.
Figure 5. HT events of Sailor. (A) The two organelle ribosomal proteins (L3 and L4) exhibited prokaryotic to eukaryotic HT events. The yellow color represents the HT characteristic of the organelle ribosomal protein L3, the dark-green color represents HT common to the organelle ribosomal proteins L3 and L4, and the light-green color represents the HT characteristic of the organelle ribosomal protein L4. (B) The two cytoplasmic ribosomal proteins (L3 and L4) exhibited HT events in prokaryotic species. The dark-green color represents HT common to the cytoplasmic ribosomal proteins L3 and L4. (C) The two cytoplasmic ribosomal proteins (L3 and L4) exhibited HT events in eukaryotic species. The yellow color represents the HT characteristic of the cytoplasm ribosomal protein L3, the dark-green color represents HT common to the cytoplasmic ribosomal proteins L3 and L4, and the light-green color represents the HT characteristic of the cytoplasm ribosomal protein L4. (D) HT based on the pairwise genetic distance comparisons of two proteins. The numbers next to the animal silhouettes represent species pairs supporting HT events in the same phylum, and the numbers behind the curve represent species pairs supporting HT events from prokaryotic to eukaryotic species.
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Table
Table 1. Taxonomic Distribution of Sailor.
Table 1. Taxonomic Distribution of Sailor.
Taxa DistributionNumber of Species Containing SailorNumber of Species Containing FL SailorNumber of Species Containing Intact SailorLength of FL SailorLength of Intact SailorTpase Length of Intact SailorTIR Length of Intact Sailor
Bacteria9441379–14371379–1437376–42223–57
Red algae11–3034–––
Land Plants1––––––
Stramenopiles23871757–44411757–4441323–50724–57
Amoebozoa2––––––
Ichthyosporea1––––––
Choanoflagellata1––––––
Fungi12222427–69792427–6979368–60752–1362
Porifera11–4115–––
Mollusca17422220–24652220–2465338–43234–237
Annelida1111927192742927
Nematoda12212754275745224
Arthropoda17465411799–44081799–4408334–67618–61
Echinodermata1112763276333428
Description of Sailor elements in 14 lineages, including the number of species with these elements, full-length (FL) elements, amino acid (aa) length of the transposase (Tpase), and length of terminal inverse repeats (TIRs).
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Shi, S.; Puzakov, M.; Guan, Z.; Xiang, K.; Diaby, M.; Wang, Y.; Wang, S.; Song, C.; Gao, B. Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons. Biology 2021, 10, 1005. https://doi.org/10.3390/biology10101005

AMA Style

Shi S, Puzakov M, Guan Z, Xiang K, Diaby M, Wang Y, Wang S, Song C, Gao B. Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons. Biology. 2021; 10(10):1005. https://doi.org/10.3390/biology10101005

Chicago/Turabian Style

Shi, Shasha, Mikhail Puzakov, Zhongxia Guan, Kuilin Xiang, Mohamed Diaby, Yali Wang, Saisai Wang, Chengyi Song, and Bo Gao. 2021. "Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons" Biology 10, no. 10: 1005. https://doi.org/10.3390/biology10101005

APA Style

Shi, S., Puzakov, M., Guan, Z., Xiang, K., Diaby, M., Wang, Y., Wang, S., Song, C., & Gao, B. (2021). Prokaryotic and Eukaryotic Horizontal Transfer of Sailor (DD82E), a New Superfamily of IS630-Tc1-Mariner DNA Transposons. Biology, 10(10), 1005. https://doi.org/10.3390/biology10101005

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