IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51011-7.html
   My bibliography  Save this article

Single cell expression and chromatin accessibility of the Toxoplasma gondii lytic cycle identifies AP2XII-8 as an essential ribosome regulon driver

Author

Listed:
  • Jingjing Lou

    (Boston College)

  • Yasaman Rezvani

    (University of Massachusetts Boston
    University of Massachusetts Boston)

  • Argenis Arriojas

    (University of Massachusetts Boston)

  • Yihan Wu

    (Boston College)

  • Nachiket Shankar

    (University of Massachusetts Boston)

  • David Degras

    (University of Massachusetts Boston)

  • Caroline D. Keroack

    (Harvard University
    Brown University)

  • Manoj T. Duraisingh

    (Harvard University)

  • Kourosh Zarringhalam

    (University of Massachusetts Boston
    University of Massachusetts Boston)

  • Marc-Jan Gubbels

    (Boston College)

Abstract

Sequential lytic cycles driven by cascading transcriptional waves underlie pathogenesis in the apicomplexan parasite Toxoplasma gondii. This parasite’s unique division by internal budding, short cell cycle, and jumbled up classically defined cell cycle stages have restrained in-depth transcriptional program analysis. Here, unbiased transcriptome and chromatin accessibility maps throughout the lytic cell cycle are established at the single-cell level. Correlated pseudo-timeline assemblies of expression and chromatin profiles maps transcriptional versus chromatin level transition points promoting the cell division cycle. Sequential clustering analysis identifies functionally related gene groups promoting cell cycle progression. Promoter DNA motif mapping reveals patterns of combinatorial regulation. Pseudo-time trajectory analysis reveals transcriptional bursts at different cell cycle points. The dominant burst in G1 is driven largely by transcription factor AP2XII-8, which engages a conserved DNA motif, and promotes the expression of 44 ribosomal proteins encoding regulon. Overall, the study provides integrated, multi-level insights into apicomplexan transcriptional regulation.

Suggested Citation

  • Jingjing Lou & Yasaman Rezvani & Argenis Arriojas & Yihan Wu & Nachiket Shankar & David Degras & Caroline D. Keroack & Manoj T. Duraisingh & Kourosh Zarringhalam & Marc-Jan Gubbels, 2024. "Single cell expression and chromatin accessibility of the Toxoplasma gondii lytic cycle identifies AP2XII-8 as an essential ribosome regulon driver," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51011-7
    DOI: 10.1038/s41467-024-51011-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51011-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51011-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Klemens Engelberg & Tyler Bechtel & Cynthia Michaud & Eranthie Weerapana & Marc-Jan Gubbels, 2022. "Proteomic characterization of the Toxoplasma gondii cytokinesis machinery portrays an expanded hierarchy of its assembly and function," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Ana Vera Antunes & Martina Shahinas & Christopher Swale & Dayana C. Farhat & Chandra Ramakrishnan & Christophe Bruley & Dominique Cannella & Marie G. Robert & Charlotte Corrao & Yohann Couté & Adrian , 2024. "In vitro production of cat-restricted Toxoplasma pre-sexual stages," Nature, Nature, vol. 625(7994), pages 366-376, January.
    3. Gioele La Manno & Ruslan Soldatov & Amit Zeisel & Emelie Braun & Hannah Hochgerner & Viktor Petukhov & Katja Lidschreiber & Maria E. Kastriti & Peter Lönnerberg & Alessandro Furlan & Jean Fan & Lars E, 2018. "RNA velocity of single cells," Nature, Nature, vol. 560(7719), pages 494-498, August.
    4. Hernan Lorenzi & Asis Khan & Michael S. Behnke & Sivaranjani Namasivayam & Lakshmipuram S. Swapna & Michalis Hadjithomas & Svetlana Karamycheva & Deborah Pinney & Brian P. Brunk & James W. Ajioka & Da, 2016. "Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Huanhuan Tan & Weixu Wang & Congjin Zhou & Yanfeng Wang & Shu Zhang & Pinglan Yang & Rui Guo & Wei Chen & Jinwen Zhang & Lan Ye & Yiqiang Cui & Ting Ni & Ke Zheng, 2023. "Single-cell RNA-seq uncovers dynamic processes orchestrated by RNA-binding protein DDX43 in chromatin remodeling during spermiogenesis," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. Yanchuan Li & Huamei Li & Cheng Peng & Ge Meng & Yijun Lu & Honglin Liu & Li Cui & Huan Zhou & Zhu Xu & Lingyun Sun & Lihong Liu & Qing Xiong & Beicheng Sun & Shiping Jiao, 2024. "Unraveling the spatial organization and development of human thymocytes through integration of spatial transcriptomics and single-cell multi-omics profiling," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    3. Christoph Ziegenhain & Rickard Sandberg, 2021. "BAMboozle removes genetic variation from human sequence data for open data sharing," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Yoshiaki Yasumizu & Naganari Ohkura & Hisashi Murata & Makoto Kinoshita & Soichiro Funaki & Satoshi Nojima & Kansuke Kido & Masaharu Kohara & Daisuke Motooka & Daisuke Okuzaki & Shuji Suganami & Eriko, 2022. "Myasthenia gravis-specific aberrant neuromuscular gene expression by medullary thymic epithelial cells in thymoma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Jialiang S. Wang & Tushar Kamath & Courtney M. Mazur & Fatemeh Mirzamohammadi & Daniel Rotter & Hironori Hojo & Christian D. Castro & Nicha Tokavanich & Rushi Patel & Nicolas Govea & Tetsuya Enishi & , 2021. "Control of osteocyte dendrite formation by Sp7 and its target gene osteocrin," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    6. Lichun Ma & Sophia Heinrich & Limin Wang & Friederike L. Keggenhoff & Subreen Khatib & Marshonna Forgues & Michael Kelly & Stephen M. Hewitt & Areeba Saif & Jonathan M. Hernandez & Donna Mabry & Roman, 2022. "Multiregional single-cell dissection of tumor and immune cells reveals stable lock-and-key features in liver cancer," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. David J. Dittmar & Franziska Pielmeier & Nicholas Strieder & Alexander Fischer & Michael Herbst & Hanna Stanewsky & Niklas Wenzl & Eveline Röseler & Rüdiger Eder & Claudia Gebhard & Lucia Schwarzfisch, 2024. "Donor regulatory T cells rapidly adapt to recipient tissues to control murine acute graft-versus-host disease," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Keyong Sun & Runda Xu & Fuhai Ma & Naixue Yang & Yang Li & Xiaofeng Sun & Peng Jin & Wenzhe Kang & Lemei Jia & Jianping Xiong & Haitao Hu & Yantao Tian & Xun Lan, 2022. "scRNA-seq of gastric tumor shows complex intercellular interaction with an alternative T cell exhaustion trajectory," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Seong Eun Lee & Seongyeol Park & Shinae Yi & Na Rae Choi & Mi Ae Lim & Jae Won Chang & Ho-Ryun Won & Je Ryong Kim & Hye Mi Ko & Eun-Jae Chung & Young Joo Park & Sun Wook Cho & Hyeong Won Yu & June You, 2024. "Unraveling the role of the mitochondrial one-carbon pathway in undifferentiated thyroid cancer by multi-omics analyses," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. David G. Priest & Takeshi Ebihara & Janyerkye Tulyeu & Jonas N. Søndergaard & Shuhei Sakakibara & Fuminori Sugihara & Shunichiro Nakao & Yuki Togami & Jumpei Yoshimura & Hiroshi Ito & Shinya Onishi & , 2024. "Atypical and non-classical CD45RBlo memory B cells are the majority of circulating SARS-CoV-2 specific B cells following mRNA vaccination or COVID-19," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    11. Jeff Yat-Fai Chung & Philip Chiu-Tsun Tang & Max Kam-Kwan Chan & Vivian Weiwen Xue & Xiao-Ru Huang & Calvin Sze-Hang Ng & Dongmei Zhang & Kam-Tong Leung & Chun-Kwok Wong & Tin-Lap Lee & Eric W-F Lam &, 2023. "Smad3 is essential for polarization of tumor-associated neutrophils in non-small cell lung carcinoma," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Fabian Peisker & Maurice Halder & James Nagai & Susanne Ziegler & Nadine Kaesler & Konrad Hoeft & Ronghui Li & Eric M. J. Bindels & Christoph Kuppe & Julia Moellmann & Michael Lehrke & Christian Stopp, 2022. "Mapping the cardiac vascular niche in heart failure," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    13. Timo N. Kohler & Joachim Jonghe & Anna L. Ellermann & Ayaka Yanagida & Michael Herger & Erin M. Slatery & Antonia Weberling & Clara Munger & Katrin Fischer & Carla Mulas & Alex Winkel & Connor Ross & , 2023. "Plakoglobin is a mechanoresponsive regulator of naive pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Alek G. Erickson & Alessia Motta & Maria Eleni Kastriti & Steven Edwards & Fanny Coulpier & Emy Théoulle & Aliia Murtazina & Irina Poverennaya & Daniel Wies & Jeremy Ganofsky & Giovanni Canu & Francoi, 2024. "Motor innervation directs the correct development of the mouse sympathetic nervous system," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Yan Tang & David J. Kwiatkowski & Elizabeth P. Henske, 2022. "Midkine expression by stem-like tumor cells drives persistence to mTOR inhibition and an immune-suppressive microenvironment," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    16. Jun Dai & Shuyu Zheng & Matías M. Falco & Jie Bao & Johanna Eriksson & Sanna Pikkusaari & Sofia Forstén & Jing Jiang & Wenyu Wang & Luping Gao & Fernando Perez-Villatoro & Olli Dufva & Khalid Saeed & , 2024. "Tracing back primed resistance in cancer via sister cells," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    17. Ryuki Shimada & Yuzuru Kato & Naoki Takeda & Sayoko Fujimura & Kei-ichiro Yasunaga & Shingo Usuki & Hitoshi Niwa & Kimi Araki & Kei-ichiro Ishiguro, 2023. "STRA8–RB interaction is required for timely entry of meiosis in mouse female germ cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Cathy Pichol-Thievend & Oceane Anezo & Aafrin M. Pettiwala & Guillaume Bourmeau & Remi Montagne & Anne-Marie Lyne & Pierre-Olivier Guichet & Pauline Deshors & Alberto Ballestín & Benjamin Blanchard & , 2024. "VC-resist glioblastoma cell state: vessel co-option as a key driver of chemoradiation resistance," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    19. Maura Galimberti & Maria R. Nucera & Vittoria D. Bocchi & Paola Conforti & Elena Vezzoli & Matteo Cereda & Camilla Maffezzini & Raffaele Iennaco & Andrea Scolz & Andrea Falqui & Chiara Cordiglieri & M, 2024. "Huntington’s disease cellular phenotypes are rescued non-cell autonomously by healthy cells in mosaic telencephalic organoids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    20. Susana I. Ramos & Zarmeen M. Mussa & Elisa N. Falk & Balagopal Pai & Bruno Giotti & Kimaada Allette & Peiwen Cai & Fumiko Dekio & Robert Sebra & Kristin G. Beaumont & Alexander M. Tsankov & Nadejda M., 2022. "An atlas of late prenatal human neurodevelopment resolved by single-nucleus transcriptomics," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51011-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.