Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus

Abstract

BackgroundRecent evidence suggests that horizontal transfer plays a significant role in the evolution of of transposable elements (TEs) in eukaryotes. Many cases of horizontal TE transfer (HTT) been reported in animals and plants, however surprisingly few examples of HTT have been reported in fungi.FindingsHere I report evidence for a novel HTT event in fungi involving Tsu4 in Saccharomyces paradoxus based on (i) unexpectedly high similarity between Tsu4 elements in S. paradoxus and S. uvarum, (ii) a patchy distribution of Tsu4 in S. paradoxus and general absence from its sister species S. cerevisiae, and (iii) discordance between the phylogenetic history of Tsu4 sequences and species in the Saccharomyces sensu stricto group. Available data suggests the HTT event likely occurred somewhere in the Nearctic, Neotropic or Indo-Australian part of the S. paradoxus species range, and that a lineage related to S. uvarum or S. eubayanus was the likely donor species. The HTT event has led to massive proliferation of Tsu4 in the South American lineage of S. paradoxus, which exhibits partial reproductive isolation with other strains of this species because of multiple reciprocal translocations. Full-length Tsu4 elements are associated with both breakpoints of one of these reciprocal translocations.ConclusionsThis work shows that comprehensive analysis of TE sequences in essentially-complete genome assemblies derived from long-read sequencing provides new opportunities to detect HTT events in fungi and other organisms. This work also provides support for the hypothesis that HTT and subsequent TE proliferation can induce genome rearrangements that contribute to post-zygotic isolation in yeast.Electronic supplementary materialThe online version of this article (10.1186/s13100-018-0122-7) contains supplementary material, which is available to authorized users.

The effect of hybridization on transposable element accumulation in an undomesticated fungal species

“…Although they were clearly distinct, Ty4 and Tsu4 LTRs showed a close relatedness, which justified their combination into the Ty4/Tsu4 family. No Tsu4 LTR was annotated in the SpA genome, consistent with this family being specific to North American S. paradoxus and absent from Eurasian S. paradoxus (Bergman, 2018). paradoxus lineages based on genome-wide SNPs.…”

“…To investigate the TE content and dynamics in North American S. paradoxus pure and hybrid lineages, we annotated six highly contiguous whole-genome assemblies previously generated from Oxford Nanopore long reads (PRJNA514804) (Eberlein et al, 2019). We used a database comprising reference sequences for S. cerevisiae Ty1, Ty2, Ty3, Ty4 and Ty5 families, along with S. paradoxus Ty3-related Ty3p (Carr et al, 2012) and Ty4-related Tsu4, the latter originating from a horizontal transfer from the Saccharomyces eubayanus/Saccharomyces uvarum clade to S. paradoxus (Bergman, 2018). These annotations revealed counts of fulllength elements an order of magnitude lower than solo LTRs (Figure 2c, Figure 2-figure supplement 1), consistent with previously reported data on S. cerevisiae and S. paradoxus (Carr et al, 2012;Goffeau et al, 1996;Kim et al, 1998;Yue et al, 2017).…”

“…RepeatMasker version open-4.0.7 (Smit et al, 2015) with parameters -s -low -gccalc and the library of reference LTR and internal sequences assembled by (Carr et al, 2012) (containing Ty1, Ty2, Ty3, Ty4 and Ty5 from S. cerevisiae and Ty3p from S. paradoxus), additionned with Tsu4 from S. uvarum (Bergman, 2018). RepeatMasker output was defragmented using REannotate version 26.11.2007(Pereira, 2008 with parameters -s 15000 -d 10000, yielding defragmented elements classified as full-length, solo LTR, truncated or orphan internal sequences.…”

Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination

“…HGAP assemblies for the genomes reported here plus a complementary set of HGAP assemblies from S. cerevisiae, S. paradoxus, and the outgroup species S. jurei [18,43] were used to identify Ty elements using a modified strategy similar to Carr et al [13]. RepeatMasker (version 4.0.5; options: -e wublast -s -xsmall -nolow -no_is) (http://repeatmasker.org) was used to find all Ty fragments with similarity to a custom database of canonical Ty sequences derived from those reported in Carr et al [13] that was updated to fix several small errors and include a version of the Tsu4 element from S. paradoxus [19] (S6 File). Inspection of raw RepeatMasker results identified a number of false positive matches to divergent sequences, LTR fragments from full-length or truncated elements were labeled as the incorrect family, tandem duplications of Ty elements that share a common LTR sequence that were incorrectly joined, and fusion of nearby solo LTRs fragments to full or truncated Ty elements.…”

“…The complete sequencing of the yeast genome provided the first insight into organization and evolution of retrotransposons at the genomic scale [6][7][8][9][10]. More recently, advances in sequencing technologies and bioinformatics have provided unprecedented opportunities to investigate the evolutionary dynamics and consequences of transposition across yeast populations and species [11][12][13][14][15][16][17][18][19][20].…”