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The Tritryps Comparative Repeatome: Insights on Repetitive Element Evolution in Trypanosomatid Pathogens

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The Tritryps Comparative Repeatome: Insights on Repetitive Element Evolution in Trypanosomatid Pathogens GBE The Tritryps Comparative Repeatome: Insights on Repetitive Element Evolution in Trypanosomatid Pathogens Sebastian Pita1,2,FlorenciaDıaz-Viraque1, Gregorio Iraola3,4, and Carlos Robello1,5,* 1Laboratory of Host Pathogen Interactions, Unidad de Biologıa Molecular, Institut Pasteur de Montevideo, Montevideo, Uruguay 2Seccion Genetica Evolutiva, Facultad de Ciencias, Universidad de la Republica, Montevideo, Uruguay 3Microbial Genomics Laboratory, Institut Pasteur Montevideo, Montevideo, Uruguay 4Centro de Biologıa Integrativa, Universidad Mayor, Santiago de Chile, Chile Downloaded from https://academic.oup.com/gbe/article-abstract/11/2/546/5306335 by guest on 31 July 2019 5Departamento de Bioquımica, Facultad de Medicina, Universidad de la Republica, Montevideo, Uruguay *Corresponding author: E-mail: [email protected]. Accepted: February 1, 2019 Data deposition: This project has been deposited at NCBI under the accesion SRP155233 Abstract The major human pathogens Trypanosoma cruzi, Trypanosoma brucei,andLeishmania major are collectively known as the Tritryps. The initial comparative analysis of their genomes has uncovered that Tritryps share a great number of genes, but repetitive DNA seems to be extremely variable between them. However, the in-depth characterization of repetitive DNA in these pathogens has been in part neglected, mainly due to the well-known technical challenges of studying repetitive sequences from de novo assemblies using short reads. Here, we compared the repetitive DNA repertories between the Tritryps genomes using genome-wide, low- coverage Illumina sequencing coupled to RepeatExplorer analysis. Our work demonstrates that this extensively implemented ap- proach for studying higher eukaryote repeatomes is also useful for protozoan parasites like trypanosomatids, as we recovered previously observed differences in the presence and amount of repetitive DNA families. Additionally, our estimations of repetitive DNA abundance were comparable to those obtained from enhanced-quality assemblies using longer reads. Importantly, our methodology allowed us to describe a previously undescribed transposable element in Leishmania major (TATE element), highlight- ing its potential to accurately recover distinctive features from poorly characterized repeatomes. Together, our results support the application of this low-cost, low-coverage sequencing approach for the extensive characterization of repetitive DNA evolutionary dynamics in trypanosomatid and other protozoan genomes. Key words: trypanosomatids, Tritryps, repetitive DNA, RepeatExplorer, RepeatExplorer, transposable elements. Main Text tissues, and distinct disease pathogenesis in mammalian Collectively known as the “Tritryps,” the unicellular mono- hosts (Jackson 2015). flagellated protozoan parasites Trypanosoma cruzi, The genomes of T. cruzi, T. brucei,andL. major have been Trypanosoma brucei,andLeishmania major are the causative initially sequenced and compared with better understand agents of American trypanosomiasis, cutaneous leishmania- gene evolution and genetic variation in these related patho- sis, and African tryrpanosomiasis, respectively. These dixe- gens (Ghedin et al. 2004; El-Sayed, Myler, Blandin, et al. nous parasites belong to the family Trypanosomatidae, 2005). A remarkable finding derived from the comparative within the order Kinetoplastida (Votypka et al. 2015). analysis of Tritryps genomes was the great number of shared Despite Tritryps share many general characteristics which genes (El-Sayed, Myler, Blandin, et al. 2005). However, the are used as distinctive taxonomic markers (i.e., their unique repetitive DNA was extremely different in these species. mitochondria known as kinetoplast), each species has its own Repetitive DNA sequences are scarce in the L. major genome, insect vector, particular life-cycle features, different target but comprises up to half of the T. cruzi genome. Moreover, ß The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 546 Genome Biol. Evol. 11(2):546–551. doi:10.1093/gbe/evz017 Advance Access publication February 4, 2019 Tritryps Comparative Repeatome GBE L. major is believed to be devoid of active transposable ele- clusters for T. cruzi, T. brucei,andL. major, respectively. In ments (TEs) (Ghedin et al. 2004; Ivens et al. 2005; Bringaud T. cruzi, we estimated that 51.25% of the genome corre- et al. 2006), but both T. cruzi and T. brucei genomes harbor sponds to repetitive DNA sequences. Out of them, 28.81% intact and autonomous TEs (Wickstead et al. 2003; El-Sayed, were annotated as coding sequences belonging to multigenic Myler, Bartholomeu, et al. 2005; Bringaud et al. 2008; families, 8.85% as LINEs (Long Interspersed Elements), 3.73% Thomas et al. 2010; Berna et al. 2018). Caused by this intrinsic as DIRS-like or tyrosin recombinase (YR) elements (mostly genome complexity—abundance of repetitive sequences and VIPER element), 3.48% as satellite DNA, 0.31% represented genes organized in tandem—the T. cruzi genome remained ribosomal DNA (rDNA), and 5.07% remained as undeter- fragmented even through long-read sequencing (1,142 and mined repeats. Conversely, in T. brucei, only 20.69% of the 599 scaffolds in hybrid and nonhybrid strains, respectively; genome harbors repetitive DNA sequences. Out of them, we Downloaded from https://academic.oup.com/gbe/article-abstract/11/2/546/5306335 by guest on 31 July 2019 Berna et al. 2018), and all of the T. cruzi sequencing projects were able to determine that 9.53% belong to coding sequen- based on short reads have demonstrated that genome assem- ces from multigenic families, 5.67% to LINE TEs, 3.59% were bly and downstream comparative analyses are extremely chal- satellite DNA repeats, 0.33% as rDNA, and 1.57% of the lenging in this species. genome remained as undetermined repeats. Finally, the re- Genome annotation procedures are mainly focused on petitive DNA fraction in L. major was smaller than in the genus standard genetic elements, frequently neglecting repetitive Trypanosoma, corresponding only to 8.80% of the genome. sequences due to their hard-achieving de novo assembly The vast majority of this repetitive DNA consisted in multigenic (Treangen and Salzberg 2012). As a consequence, repetitive families (see details later), which reached the 3.93% of the DNA is poorly described and studied (Altemose et al. 2014). In genome. Additionally, 1.32% was identified as TEs named this context, RepeatExplorer has emerged as a widely used telomere-associated mobile elements (TATEs), 0.29% as approach to comprehensively evaluate the nature of repetitive LINE TEs, and 0.27% assigned to satellite DNA repeats. In sequences. This bioinformatic tool attempts to cluster low- addition, several clusters belonged to rDNA genes and coverage high-throughput sequencing reads using a graph- snoRNA regions, which accounted for the 0.57% and based algorithm to characterize and quantify the complete 0.34% of the genome, respectively. The remaining 2.09% repetitive DNA fraction of a genome (Novak et al. 2010, of the genome was annotated as undetermined repeats 2013, 2017), which nowadays is known as the “repeatome” (fig. 1). In terms of quantitative comparison, figure 2 is repre- (Maumus and Quesneville 2014). Low-coverage sequencing is senting the total amount of genome content in mega base a cost-effective approach that does not require having previ- pairs (Mbp), depicting the repetitive and nonrepetitive ous information about the target genome and avoids dealing sequences. Although difference in genome size on Tritryps with whole-genome assemblies. Beyond RepeatExplorer was is highly influenced by the repetitive DNA content, it does originally conceived to analyze plant repeatomes, it has been not the only responsible, since nonrepetitive DNA fraction successfully applied in mammals (Pagan et al. 2012), insects abundance is quite different in each genome. (Ruiz-Ruano et al. 2016; Palacios-Gimenez et al. 2017; Pita In agreement to previous quantification of repetitive DNA et al. 2017), and fishes (Utsunomia et al. 2017). Here, we used in the genomes of T. cruzi CL Brener (El-Sayed, Myler, low-coverage sequencing and the RepeatExplorer approach Bartholomeu, et al. 2005), Sylvio X-10 (Franzen et al. 2011), to compare the repeatomes of T. cruzi, T. brucei,andL. major Dm28c and TCC (Berna et al. 2018) strains, our current anal- to reference genomes. Four genomes of T. cruzi—with differ- ysis showed that almost half of the genome is composed by ent sequencing technology approaches—were compared. CL these sequences. Within the repetitive fraction, the most Brenner strain with BAC-end Sanger sequencing (El-Sayed, abundant sequences correspond to multigenic families as pre- Myler, Bartholomeu, et al. 2005), Sylvio X10 strain with 454 viously described on reference genomes. However, the rela- technology (Franzen et al. 2011), and the newly less collapsed tive abundance of each family remained uncertain and PacBio sequenced strains Dm28c and TCC (Berna et al. 2018). probably underestimated (El-Sayed, Myler, Bartholomeu, The extensive amplification of repeated DNA is the main rea- et al. 2005). It was only with the upcoming of the new ref- son why the T. cruzi genomes
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