Differences in N6-methyladenosine (m6A) methylation among the three major clonal lineages of Toxoplasma gondii tachyzoites

doi:10.1016/j.jia.2024.03.072

Journal of Integrative Agriculture

2025, Vol. 24

Issue (7): 2810-2825 DOI: 10.1016/j.jia.2024.03.072

Animal Science · Veterinary Medicine

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Differences in N⁶-methyladenosine (m⁶A) methylation among the three major clonal lineages of Toxoplasma gondii tachyzoites

Changning Wei¹, Hui Cao¹, Chenxu Li¹, Hongyu Song¹, Qing Liu¹, Xingquan Zhu^{1, 2#}, Wenbin Zheng^1#

¹Laboratory of Parasitic Diseases, College of Veterinary Medicine, Shanxi Agricultural University, Taigu 030801, China

²Key Laboratory of Veterinary Public Health of Higher Education of Yunnan Province, College of Veterinary Medicine, Yunnan Agricultural University, Kunming 650201, Chinatory of Livestock Biology, Northwest A&F University, Yangling 712100, China

Highlights
● Providing the first comprehensive comparison of m⁶A methylation profiles among the three major clonal lineages (Types I, II and III) of Toxoplasma gondii.
● Distinct m⁶A methylation patterns across different T. gondii genotypes reveal molecular mechanisms underlying genotype-specific virulence.
● Providing new insights into the molecular basis of virulence differences between T. gondii genotypes.

Abstract
References

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摘要

刚地弓形虫（Toxoplasma gondii）呈全球性分布，可感染人和几乎所有的温血动物，引起人兽共患弓形虫病。弓形虫仅有一个种，但存在有200多种基因型，不同基因型虫株具有不同的地理分布和毒力差异。N⁶-腺苷酸甲基化（N⁶-methyladenosine, m⁶A）是mRNAs中丰度最高的表观遗传修饰形式，其涉及mRNAs生物学的多种方面，然而目前尚不清楚弓形虫不同基因型之间的mRNA m⁶A甲基化修饰的差异。因此，本研究采用RNA测序（RNA-seq）和m⁶A甲基化测序（MeRIP-seq）技术，来探索弓形虫三个主要克隆谱系（I型、II型和III型）之间mRNA m⁶A甲基化修饰的差异，并鉴定不同基因型之间主要的差异性表达的甲基化基因。结果表明，在弓形虫RH（I型）、ME49（II型）和VEG（III型）虫株速殖子的5211、5607和4974个基因上分别鉴定出7650、8359和7264个m⁶A甲基化修饰峰；大多数的m⁶A甲基化修饰发生在3'UTR区，其次是CDS区，且在3'UTR区发生m⁶A甲基化修饰的基因具有较高的mRNA丰度。通过RH vs. ME49、RH vs. VEG和ME49 vs. VEG组间对比，在676、168和553个基因上分别鉴定出735、192和615个差异甲基化峰。进一步结合不同基因型之间的RNA-seq数据分析发现，在RH vs. ME49、RH vs. VEG和ME49 vs. VEG三个比较组中分别鉴定出172、41和153个差异性表达的甲基化基因，且大多数差异性表达的甲基化基因的m⁶A修饰水平与mRNA丰度之间呈正相关性。对这些差异性表达的甲基化基因进行GO注释分析发现，其主要参与Golgi apparatus、plasma membrane、signal transduction、RNA processing和catalytic step 2 spliceosome等生物学途径；对这些差异性表达的甲基化基因进行KEGG通路富集分析表明，其主要参与endocytosis、systemic lupus erythematosus和mTOR signaling pathway等信号通路。这些发现揭示了m⁶A甲基化修饰在弓形虫不同基因型虫株之间存在特异性差异，有助于更好地研究m⁶A甲基化修饰在弓形虫病理生物学中的作用，阐明弓形虫不同基因型虫株之间毒力差异的分子机制。

Abstract

Toxoplasma gondii is an important zoonotic parasite which has over 200 genotypes worldwide. N⁶-methyladenosine (m⁶A) methylation is a common epigenetic modification in messenger RNAs (mRNAs), and has been implicated in many aspects of mRNA biology. However, little is known about the difference in m⁶A methylation among different genotypes of T. gondii. In the present study, we employed methylated RNA immunoprecipitation sequencing (MeRIP-seq) technology to identify key genes exhibiting m⁶A methylation in the three major clonal lineages (Types I, II and III) of T. gondii tachyzoites. A total of 7,650, 8,359 and 7,264 m⁶A peaks were identified in 5,211, 5,607 and 4,974 genes in tachyzoites of RH (Type I), ME49 (Type II) and VEG strain (Type III), respectively. By comparing RH vs. ME49, RH vs. VEG, and ME49 vs. VEG, 735, 192 and 615 differentially methylated peaks (DMPs) were identified in 676, 168 and 553 genes, respectively. A combined MeRIP-seq and RNA-seq analysis revealed 172, 41 and 153 differentially methylated genes (DMGs) at both the m⁶A methylation and transcriptional level. Gene Ontology term enrichment analysis of the DMPs identified differences related to Golgi apparatus, plasma membrane, signal transduction, RNA processing and catalytic step 2 spliceosome. KEGG pathway enrichment analysis showed that the DMGs are mainly involved in endocytosis, systemic lupus erythematosus and mTOR signaling pathway. These findings reveal genotype-specific differences in m⁶A methylation, which provide new resources for further investigations of the role of m⁶A in the pathobiology of T. gondii.

Keywords: Toxoplasma gondii toxoplasmosis MeRIP-seq RNA-seq N⁶-methyladenosine

Received: 11 October 2023 Online: 27 March 2024 Accepted: 02 March 2024

Fund: This work was supported by the National Key Research and Development Program of China (2021YFC2300800, 2021YFC2300802 and 2021YFC2300804), the NSFC-Yunnan Joint Fund, China (U2202201), the Research Fund of Shanxi Province for Introduced High-level Leading Talents, China (RFSXIHLT202101), the Special Research Fund of Shanxi Agricultural University for High-level Talents, China (2021XG001), and the Veterinary Public Health Innovation Team of Yunnan Province, China (202105AE160014).

About author: #Correspondence Xingquan Zhu, Tel: +86-354-6286886, E-mail: xingquanzhu1@hotmail.com; Wenbin Zheng, Tel: +86-354-6286166, E-mail: wenbinzheng1@126.com

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Changning Wei, Hui Cao, Chenxu Li, Hongyu Song, Qing Liu, Xingquan Zhu, Wenbin Zheng. 2025. Differences in N⁶-methyladenosine (m⁶A) methylation among the three major clonal lineages of Toxoplasma gondii tachyzoites. Journal of Integrative Agriculture, 24(7): 2810-2825.

Amouei A, Sarvi S, Sharif M, Aghayan S A, Javidnia J, Mizani A, Moosazadeh M, Shams N, Hosseini S A, Hosseininejad Z, Nayeri Chegeni T, Badali H, Daryani A. 2020. A systematic review of Toxoplasma gondii genotypes and feline: Geographical distribution trends. Transboundary and Emerging Diseases, 67, 46–64.

Alvarez C A, S uvorova E S. 2017. Checkpoints of apicomplexan cell division identified in Toxoplasma gondii. PLoS Pathogens, 13, e1006483.

Baumgarten S, Bryant J M, Sinha A, Reyser T, Preiser P R, Dedon P C, Scherf A. 2019. Transcriptome-wide dynamics of extensive m6A mRNA methylation during Plasmodium falciparum blood-stage development. Nature Microbiology, 4, 2246–2259.

B eemon K, Keith J. 1977. Localization of N6-methyladenosine in the Rous sarcoma virus genome. Journal of Molecular Biology, 113, 165–179.

Berlivet S, Scutenaire J, Deragon J M, Bousquet-Antonelli C. 2019. Readers of the m6A epitranscriptomic code. Biochimica et Biophysica Acta-Gene Regulatory Mechanisms, 1862, 329–342.

Chaichan P, Mercier A, Galal L, Mahittikorn A, Ariey F, Morand S, Boumediene F, Udonsom R, Hamidovic A, Murat J B, Sukthana Y, Darde M L. 2017. Geographical distribution of Toxoplasma gondii genotypes in Asia: A link with neighboring continents. Infection, Genetics and Evolution, 53, 227–238.

Chen S, Zhou Y, Chen Y, Gu J. 2018. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884–i890.

Cong W, Zhang N Z, Hu R S, Zou F C, Zou Y, Zhong W Y, Wu J J, Fallaize C J, Zhu X Q, Elsheikha H M. 2020. Prevalence, risk factors and genotype distribution of Toxoplasma gondii DNA in soil in China. E cotoxicology and Environmental Safety, 189, 109999.

Crawford J, Grujic O, Bruic E, Czjzek M, Grigg M E, Boulanger M J. 2009. Structural characterization of the bradyzoite surface antigen (BSR4) from Toxoplasma gondii, a unique addition to the surface antigen glycoprotein 1-related superfamily. Journal of Biological Chemistry, 284, 9192–9198.

Dang Y, Dong Q, Wu B, Yang S, Sun J, Cui G, Xu W, Zhao M, Zhang Y, Li P, Li L. 2022. Global landscape of m6A methylation of differently expressed genes in muscle tissue of Liaoyu white cattle and simmental cattle. Frontiers in Cell and Developmental Biology, 10, 840513.

Deng X, Chen K, Luo G Z, Weng X, Ji Q, Zhou T, He C. 2015. Widespread occurrence of N6-methyladenosine in bacterial mRNA. Nucleic Acids Research, 43, 6557–6567.

Dubey J P. 2022. Toxoplasmosis of Animals And Humans. 3rd ed. CRC Press, Boca Raton, Florida.

Dubin D T, Taylor R H. 1975. The methylation state of poly A-containing messenger RNA from cultured hamster cells. Nucleic Acids Research, 2, 1653–1668.

English E D, Striepen B. 2019. T he cat is out of the bag: How parasites know their hosts. PLoS Biology, 17, e3000446.

Elsheikha H M, Marra C M, Z hu X Q. 2021. Epidemiology, pathophysiology, diagnosis, and management of cerebral toxoplasmosis. Clinical Microbiology Reviews, 34, e 00115–e00119.

Fang S, Peng B, Wen Y, Yang J, Wang H, Wang Z, Qian K, Wei Y, Jiao Y, Gao C, Dou L. 2022. Transcriptome-wide analysis of RNA N6-m ethyladenosine modification in adriamycin-resistant acute myeloid leukemia cells. Frontiers in Genetics, 13, 833694.

Farhat D C, Bowler M W, Communie G, Pontier D, Belmudes L, Mas C, Corrao C, Coute Y, Bougdour A, Lagrange T, Hakimi M A, Swale C. 2021. A plant-like mechanism coupling m6A reading to polyadenylation safeguards transcriptome integrity and developmental gene partitioning in Toxoplasma. eLife, 10, e68312.

Frye M, Harada B T, Behm M, He C. 2018. RNA modifications modulate gene expression during development. Science, 361, 1346–1349.

Hassan M A, Melo M B, Haas B, Jensen K D, Saeij J P. 2012. De novo reconstruction of the Toxoplasma gondii transcriptome improves on the current genome annotation and reveals alternatively spliced transcripts and putative long non-coding RNAs. BMC Genomics, 13, 696.

He C, Xu M Z, Pan S, Wang H, Peng H J, Liu Z Z. 2020. iTRAQ-based phosphoproteomic analysis of Toxoplasma gondii tachyzoites provides insight into the role of phosphorylation for its invasion and egress. Frontiers in Cellular and Infection Microbiology, 10, 586466.

He Y, Li L, Yao Y, Li Y, Zhang H, Fan M. 2021. Transcriptome-wide N6-methyladenosine (m6A) methylation in watermelon under CGMMV infection. BMC Plant Biology, 21, 516.

Heinz S, Benner C, Spann N, Bertolino E, Lin Y C, Laslo P, Cheng J X, Murre C, Singh H, Glass C K. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell, 38, 576–589.

H olmes M J, Padgett L R, Bastos M S, Sullivan Jr W J. 2021. m6A RNA methylation facilitates pre-mRNA 3´-end formation and is essential for viability of Toxoplasma gondii. PLoS Pathogens, 17, e1009335.

Howe D K, Sibley L D. 1995. Toxoplasma gondii comprises three clonal lineages: Correlation of parasite genotype with human disease. Journal of Infectious Diseases, 172, 1561–1566.

Lan Q, Liu P Y, Bell J L, Wang J Y, Huttelmaier S, Zhang X D, Zhang L, Liu T. 2021. The emerging roles of RNA m6A methylation and demethylation as critical regulators of tumorigenesis, drug sensitivity, and resistance. Cancer Research, 81, 3431–3440.

Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357–359.

Li F C, Nie L B, Elsheikha H M, Yin F Y, Zhu X Q. 2021. Lysine crotonylation is widespread on proteins of diverse functions and localizations in Toxoplasma gondii. Parasitology Research, 120, 1617–1626.

Li N, Guo Q, Zhang Q, Chen B J, Li X A, Zhou Y. 2022. C omprehensive analysis of differentially expressed profiles of mRNA N6-methyladenosine in colorectal cancer. Frontiers in Cell and Developmental Biology, 9, 760912.

Lin X, Chai G, Wu Y, Li J, Chen F, Liu J, Luo G, Tauler J, Du J, Lin S, He C, Wang H. 2019. RNA m6A methylation regulates the epithelial mesenchymal transition of cancer cells and translation of Snail. Nature Communications, 10, 2065.

Liu L, Zeng S, Jiang H, Zhang Y, Guo X, Wang Y. 2019. Differential m6A methylomes between two major life stages allows potential regulations in Trypanosoma brucei. B iochemical and Biophysical Research Communications, 508, 1286–1290.

Liu Z, Chen X, Zhang P, Li F, Zhang L, Li X, Huang T, Zheng Y, Yu T, Zhang T, Zeng W, Lu H, Lv Y. 2021. Transcriptome-wide dynamics of m6A mRNA methylation during porcine spermatogenesis. G enomics Proteomics Bioinformatics, 21, 729–741.

Lourido S. 2019. Toxoplasma gondii. Trends in Parasitology, 35, 944–945.

Love M I, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.

Matta S K, Rinkenberger N, Dunay I R, Sibley L D. 2021. Toxoplasma gondii infection and its implications within the central nervous system. Nature Reviews Microbiology, 19, 467–480.

Meng J, Lu Z, Liu H, Zhang L, Zhang S, Chen Y, Rao M K, Huang Y. 2014. A protocol for RNA methylation differential analysis with MeRIP-Seq data and exomePeak R/Bioconductor package. Methods, 69, 274–281.

Montazeri M, Mehrzadi S, Sharif M, Sarvi S, Tanzifi A, Aghayan S A, Daryani A. 2018. Drug resistance in Toxoplasma gondii. Frontiers in Microbiology, 9, 2587.

Nie L B, Liang Q L, Du R, Elsheikha H M, Han N J, Li F C, Zhu X Q. 2020. Global proteomic analysis of lysine malonylation in Toxoplasma gondii. Frontiers in Microbiology, 11, 776.

Perry R P, Kelley D E, Friderici K, Rottman F. 1975. The methylated constituents of L cell messenger RNA: Evidence for an unusual cluster at the 5´ terminus. Cell, 4, 387–394.

Pertea M, Pertea G M, Antonescu C M, Chang T C, Mendell J T, Salzberg S L. 2015. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33, 290–295.

du Plooy I, Mlangeni M, Christian R, Tsotetsi-Khambule A M. 2023. An African perspective on the genetic diversity of Toxoplasma gondii: A systematic review. Parasitology, 150, 551–578.

Saeij J P, Boyle J P, Boothroyd J C. 2005. Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends in Parasitology, 21, 476–481.

Schwartz S, Agarwala S D, Mumbach M R, Jovanovic M, Mertins P, Shishkin A, Tabach Y, Mikkelsen T S, Satija R, Ruvkun G, Carr S A, Lander E S, Fink G R, Regev A. 2013. High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis. Cell, 155, 1409–1421.

Sendinc E, Shi Y. 2023. RNA m6A methylation across the transcriptome. M olecular Cell, 83, 428–441.

Shen L, Liang Z, Gu X, Chen Y, Teo Z W, Hou X, Cai W M, Dedon P C, Liu L, Yu H. 2016. N6-methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis. Developmental Cell, 38, 186–200.

Shulman Z, Stern-Ginossar N. 2020. T he RNA modification N6-methyladenosine as a novel regulator of the immune system. Nature Immunology, 21, 501–512.

Shwab E K, Saraf P, Zhu X Q, Zhou D H, McFerrin B M, Ajzenberg D, Schares G, Hammond-Aryee K, van Helden P, Higgins S A, Gerhold R W, Rosenthal B M, Zhao X, Dubey J P, Su C. 2018. Human impact on the diversity and virulence of the ubiquitous zoonotic parasite Toxoplasma gondii. Proceedings of The National Academy of Sciences of the United States of America, 115, E6956–E6963.

Shwab E K, Zhu X Q, Majumdar D, Pena H F, Gennari S M, Dubey J P, Su C. 2014. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology, 141, 453–461.

Sibley L D, Boothroyd J C. 1992. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature, 359, 82–85.

Thorvaldsdóttir H, Robinson J T, Mesirov J P. 2013. Integrative genomics viewer (IGV): High-performance genomics data visualization and exploration. Briefings in Bioinformatics, 14, 178–192.

Vitaliano S N, Soares H S, Minervino A H, Santos A L, Werther K, Marvulo M F, Siqueira D B, Pena H F, Soares R M, Su C, Gennari S M. 2014. Genetic characterization of Toxoplasma gondii from Brazilian wildlife revealed abundant new genotypes. International Journal for Parasitology-Parasites and Wildlife, 3, 276–283.

Wang K, Li M, Hakonarson H. 2010. AN NOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nu cleic Acids Research, 38, e164.

Wang Z D, Liu H H, Ma Z X, Ma H Y, Li Z Y, Yang Z B, Zhu X Q, Xu B, Wei F, Liu Q. 2017. Toxoplasma gondii infection in immunocompromised patients: A systematic review and meta-analysis. Frontiers in Microbiology, 8, 389.

Wu J, Mao X, Cai T, Luo J, Wei L. 2006. KOBAS server: A web-based platform for automated annotation and pathway identification. Nucleic Acids Research, 34, W720–W724.

Yan H, Zhang L, Cui X, Zheng S, Li R. 2022. Roles and mechanisms of the m6A reader YTHDC1 in biological processes and diseases. Cell Death Discovery, 8, 237.

Yang X, Wang J, Ma X, Du J, Mei C, Zan L. 2021. Tr anscriptome-wide N6-methyladenosine methylome profiling reveals m6A regulation of skeletal myoblast differentiation in cattle (Bos taurus). Frontiers in Cell and Developmental Biology, 9, 785380.

Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biology and Evolution, 11, R14.

Yue H, Nie X, Yan Z, Weining S. 2019. N6 -methyladenosine regulatory machinery in plants: Composition, function and evolution. Plant Biotechnology Journal, 17, 1194–1208.

Zhou C X, Zhu X Q, Elsheikha H M, He S, Li Q, Zhou D H, Suo X. 2016. Global iTRAQ-based proteomic profiling of Toxoplasma gondii oocysts during sporulation. Journal of Proteomics, 148, 12–19.

Zhou D H, Wang Z X, Zhou C X, He S, Elsheikha H M, Zhu X Q. 2017. Comparative proteomic analysis of virulent and avirulent strains of Toxoplasma gondii reveals strain-specific patterns. Oncotarget, 8, 80481–80491.

Zhuang H, Yu B, Tao D, Xu X, Xu Y, Wang J, Jiao Y, Wang L. 2023. The role of m6A methylation in therapy resistance in cancer. Molecular Cancer, 22, 91.

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