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Exploring the Remote Ties Between Helitron Transposases and Other Rolling-Circle Replication Proteins

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Exploring the Remote Ties Between Helitron Transposases and Other Rolling-Circle Replication Proteins International Journal of Molecular Sciences Article Exploring the Remote Ties between Helitron Transposases and Other Rolling-Circle Replication Proteins Pedro Heringer and Gustavo C. S. Kuhn * Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, CEP 31270-901, Brazil; [email protected] * Correspondence: [email protected]; Tel.: +55-(31)-3409-3062 Received: 28 August 2018; Accepted: 7 October 2018; Published: 9 October 2018 Abstract: Rolling-circle replication (RCR) elements constitute a diverse group that includes viruses, plasmids, and transposons, present in hosts from all domains of life. Eukaryotic RCR transposons, also known as Helitrons, are found in species from all eukaryotic kingdoms, sometimes representing a large portion of their genomes. Despite the impact of Helitrons on their hosts, knowledge about their relationship with other RCR elements is still elusive. Here, we compared the endonuclease domain sequence of Helitron transposases with the corresponding region from RCR proteins found in a wide variety of mobile genetic elements. To do that, we used a stepwise alignment approach followed by phylogenetic and multidimensional scaling analyses. Although it has been suggested that Helitrons might have originated from prokaryotic transposons or eukaryotic viruses, our results indicate that Helitron transposases share more similarities with proteins from prokaryotic viruses and plasmids instead. We also provide evidence for the division of RCR endonucleases into three groups (Y1, Y2, and Yx), covering the whole diversity of this protein family. Together, these results point to prokaryotic elements as the likely closest ancestors of eukaryotic RCR transposons, and further demonstrate the fluidity that characterizes the boundaries separating viruses, plasmids, and transposons. Keywords: Helitron; rolling-circle replication; mobile genetic element; viral evolution 1. Introduction Rolling-circle replication (RCR) proteins are essential components of many genetic elements found in all three domains of life. These proteins can be classified into three different groups according to their main function: (i) Rep proteins (vegetative replication), (ii) Mob proteins/relaxases (conjugation), and (iii) transposases (transposon mobility) [1,2]. Helitrons are the eukaryotic representatives of RCR transposable elements (TEs), found in species from all eukaryotic kingdoms in highly variable copy numbers [3,4]. Their transposition is thought to occur by a mechanism similar to the one proposed for bacterial RCR TEs, like the IS91 family of elements [4–6]. Briefly, the Helitron transposase binds to the 5’-end of the element, using one of its two catalytic tyrosines to create a 50-phosphotyrosine intermediate and a free 30-OH at the donor site. The leading strand covalently bound to the transposase is displaced, the lagging strand is synthesized, and the second catalytic tyrosine nicks the 3’-end, promoting the formation of a double-strand circle intermediate. The transposase then cleaves the leading strand from the circular intermediate, but this time the second tyrosine cleaves the host’s genome, forming a free 3’-OH which attacks the first 5’-phosphotyrosine linkage. After the 3’-end of the circular intermediate is also joined to the recipient’s free 5’-end, an integrated single-strand “loop” is formed and probably resolved during the host’s genome replication. In addition, it has been recently Int. J. Mol. Sci. 2018, 19, 3079; doi:10.3390/ijms19103079 www.mdpi.com/journal/ijms Int. J. Mol. Sci. Sci. 2018, 19, x 3079 FOR PEER REVIEW 22 of of 10 the host’s genome replication. In addition, it has been recently shown that Helitron transposition shownshares mechanistic that Helitron similarities transposition with shares the replication mechanistic process similarities used bywith some the circular replication viruses process [7]. Despite used bysome some of the circular differences viruses in [7 ].their Despite mode some of propagat of the differencesion, the main in their catalytic mode reaction of propagation, used by the all mainRCR catalyticelements reactionis essentially used bythe allsame RCR [1]. elements is essentially the same [1]. Helitron transposases are composed of a typicaltypical domain,domain, the endonuclease involved in the initiation of RCR (RCRE or Rep), fused to a helicase domain (Hel) from the superfamily 1 (S1H) (Figure(Figure1 1))[ [4,8].4,8]. This This protein, protein, also also known known as RepHel, as RepHel, belongs belongs to the to HUH the HUH (named (named after one after of one its ofconserved its conserved motifs motifs with withtwo twoHis Hisresidues residues sepa separatedrated by bya ahydrophobic hydrophobic residue) residue) family family of endonucleases [1]. [1]. Although Although HUH HUH endonucleases endonucleases from from eukaryotic eukaryotic viruses viruses and andsome some plasmids plasmids also alsohave havea helicase a helicase domain, domain, they belong they belongto the superfam to the superfamilyily 3 (S3H), 3which (S3H), is unrelated which is unrelatedto the one tofound the onein Helitrons. found in Helitrons.Furthermore, Furthermore, prokaryote prokaryote viruses only viruses encode only a encodeRCRE domain a RCRE with domain no withhelicase no helicase(Figure (Figure1) [8,9].1 )[8,9]. Figure 1.1. Modular diversity of HUHHUH endonucleases.endonucleases. Schematic representation of the rolling-circle replication (RCR) proteins includedincluded inin thethe presentpresent analysis.analysis. Rolling-circleRolling-circle replicationreplication endonucleaseendonuclease (RCRE)(RCRE) domainsdomains havehave thethe first first two two motifs motifs (I (I and and II), II), in in addition addition to to the the third third motif motif represented represented by by one one or twoor two tyrosines tyrosines (Y) (Y) in thein the catalytic catalytic core core (dots (dots represent represent variable variable amino amino acid acid residues). residues). Domains Domains are notare drawnnot drawn to scale, to scale, and segmentsand segments after after helicase helicase domains domains are not are represented. not represented. Based Based on information on information from Chandlerfrom Chandler et al. [1et], al. Koonin [1], Koonin and Dolja and [ 8Dolja], and [8], the and Conserved the Conserved Domain Domain Database Database (CDD) search (CDD) tool search [10]. tool [10]. Since Helitrons were discovered [11], a few preliminary suggestions about their evolutive origins haveSince been made.Helitrons These were can discovered be generally [11], divided a few in pr twoeliminary scenarios: suggestions the first suggests about their that Helitronsevolutive originatedorigins have from been a prokaryoticmade. These ancestral can be generally RCR TE di [8vided,11], and in two the secondscenarios: adds the the first possibility suggests that Helitrons originated descended from from a an prokaryotic ancient eukaryotic ancestral RCR viral TE integration [8,11], and [12 the]. Thesecond first adds scenario the possibility is mainly basedthat Helitrons on the obvious descended similarities from an in theancient mode eukaryot of propagationic viralof integration eukaryotic [12]. and prokaryoticThe first scenario RCR TEs, is whilemainly the based second on scenariothe obvious considers similarities the fact in that,the mo inde contrast of propagation to prokaryote of eu RCRkaryotic TEs, and Helitron prokaryotic coding sequencesRCR TEs, includewhile the a helicase second domainscenario and considers sometimes the a fact ssDNA-binding that, in contrast protein, to similarlyprokaryote to someRCR RCRTEs, proteinsHelitron fromcoding eukaryotic sequences viruses. include The a facthelicase that manydomain viral and copies sometimes from geminiviruses a ssDNA-binding were foundprotein, to besimilarly integrated to some in the RCR tobacco proteins genome from [13 ]eukaryotic was also used viruses. to support The fact this that hypothesis. many viral In fact, copies since from this scenariogeminiviruses was first were proposed, found to severalbe integrated studies in showedthe tobacco copies genome from [13] different was also eukaryotic used to RCRsupport viruses this inhypothesis. host chromosomes, In fact, since revealing this scenario that viral was integrations first proposed, of these several replicons studies are moreshowed common copies than from it wasdifferent previously eukaryotic thought RCR (reviewed viruses in in host [14]). chromosomes, In addition, it hasrevealing been shownthat viral that integrations several geminivirus- of these andreplicons parvovirus-related are more common sequences than it integrated was previously in eukaryote thought genomes (reviewed display in [14]). TE features,In addition, and it have has apparentlybeen shown shifted that several from a viralgeminivirus- to a transposon-like and parvov modeirus-related of replication sequences [15]. integrated in eukaryote genomes display TE features, and have apparently shifted from a viral to a transposon-like mode of replication [15]. Int. J. Mol. Sci. 2018, 19, 3079 3 of 10 Despite the above considerations, some differences between the RCR proteins of Helitrons and eukaryotic viruses argue against their evolutionary relationship. Firstly, as mentioned before, helicases from these two classes of elements belong to different superfamilies. Also, with the exception of parvoviruses [16], all RCR proteins from eukaryotic ssDNA viruses contain only one tyrosine (Y1) in their catalytic
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