Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus

Abstract

Background: Recent 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.

Findings: Here 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.

Conclusions: This 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.

Keywords: Genome rearrangement; Horizontal transfer; Transposable element; Yeast.

Fig. 1

Evolution of the Ty4/Tsu4 super-family in the Saccharomyces sensu stricto species group. a. Maximum likelihood phylogeny of all full-length Ty4 and Tsu4 elements from 12 strains of S. cerevisiae and S. paradoxus with PacBio assemblies from Yue et al. [13] plus all complete or nearly-complete Tsu4 elements identified in Saccharomyces WGS assemblies at NCBI. Labels are shown for branches in the maximum likelihood tree that are supported by ≥ 90% of bootstrap replicates. The scale bar for branch lengths is in substitutions per site, and the tree is midpoint rooted. Tsu4 sequences from hybrid strains (S. pastorianus and Saccharomyces sp. M14) were assigned to the S. eubayanus subgenome and presumed to have originated in S. eubayanus. b. Genome organization of the reciprocal translocation between chrIX and chrXV in UFRJ50816. Sequences from the standard arrangement chrIX are shown in blue, and sequences from the standard arrangement chrXV are shown in green. Protein-coding genes, tRNA genes, and solo LTRs are shown approximately to scale as solid arrows, grey rectangles and boxed arrowheads, respectively. Approximate translocation breakpoints in UFRJ50816 based on whole genome alignments can be localized to chrIX:252268-259232 and chrXV:320536-328356 (dashed lines). Full-length Tsu4 elements are present in both translocation breakpoints. The Tsu4 elements associated in the chrIX and chrXV reciprocal translocation between are denoted by asterices in panel a