Architecture, Chromatin and Gene Organization of Toxoplasma gondii Subtelomeres

Abstract

Subtelomeres (ST) are chromosome regions that separate telomeres from euchromatin and play relevant roles in various biological processes of the cell. While their functions are conserved, ST structure and genetic compositions are unique to each species. This study aims to identify and characterize the subtelomeric regions of the 13 Toxoplasma gondii chromosomes of the Me49 strain. Here, STs were defined at chromosome ends based on poor gene density. The length of STs ranges from 8.1 to 232.4 kbp, with a gene density of 0.049 genes/kbp, lower than the Me49 genome (0.15 kbp). Chromatin organization showed that H3K9me3, H2A.X, and H3.3 are highly enriched near telomeres and the 5′ end of silenced genes, decaying in intensity towards euchromatin. H3K4me3 and H2A.Z/H2B.Z are shown to be enriched in the 5′ end of the ST genes. Satellite DNA was detected in almost all STs, mainly the sat350 family and a novel satellite named sat240. Beyond the STs, only short dispersed fragments of sat240 and sat350 were found. Within STs, there were 12 functional annotated genes, 59 with unknown functions (Hypothetical proteins), 15 from multigene FamB, and 13 from multigene family FamC. Some genes presented low interstrain synteny associated with the presence of satellite DNA. Orthologues of FamB and FamC were also detected in Neospora caninum and Hammondia hammondi. A re-analysis of previous transcriptomic data indicated that ST gene expression is strongly linked to the adaptation to different situations such as extracellular passage (evolve and resequencing study) and changes in metabolism (lack of acetyl-CoA cofactor). In conclusion, the ST region of the T. gondii chromosomes was defined, the STs genes were determined, and it was possible to associate them with high interstrain plasticity and a role in the adaptability of T. gondii to environmental changes.

An apicomplexan bromodomain protein, TgBDP1, associates with diverse epigenetic factors to regulate essential transcriptional processes in Toxoplasma gondii

“…5C and D ; Table S3 ). We also observed strong enrichment of TgBDP1 at the ends of chromosomes corresponding with regions of the telomeric repeats “TTTAGGG,” but TgBDP1 binding did not extend into subtelomeric regions as defined by Contreras et al ( 32 ).…”

“…TgBDP1 also appears to be recruited to telomeric regions. Given that Toxoplasma telomeres are heterochromatic ( 32 , 51 ) and, therefore, the histones are hypoacetylated, it is unclear how TgBDP1 might be recruited to these regions. The extent of TgBDP1 enrichment at the telomeres may be artifactual due to the highly repetitive sequence structure of the telomeres that challenges accurate mapping of sequence reads, so further studies will be needed to confirm TgBDP1 binding to these regions.…”

Subtelomeric plasticity contributes to gene family expansion in the human parasitic flatworm Schistosoma mansoni

“…We found that TEs are enriched in these regions ( p < 0.001; t-test) while other repeats are not, indicating that TEs are the main contributor to repetitiveness in these regions. As low gene density is another hallmark of subtelomeres [ 70 ], we also tested gene content of S. mansoni ’s subtelomeres, and found that the mean fraction of nucleotides annotated as genes is statistically different between subtelomeres and chromosome bodies (t-test p < 0.01, Fig. 1 C) suggesting less density of genes in the former.…”

Late Embryogenesis Abundant Proteins Contribute to the Resistance of Toxoplasma gondii Oocysts against Environmental Stresses

“…We realized that in T. gondii , N. caninum , and B. besnoiti , for which the available genome information includes the respective telomeric end, the LEA genes are subtelomeric, being located between 6.6 kb ( N. caninum ) up to 201 kb ( T. gondii ) upstream of the telomer ( Fig. 1A ) ( 65 ). Note that the annotated syntenies on ToxoDB (release 59) are not entirely correct ( Fig.…”