IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51761-4.html
   My bibliography  Save this article

Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes

Author

Listed:
  • Hong-Yan Wang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Jian-Yang Chen

    (BGI Research
    BGI Research)

  • Yanan Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center
    Shanghai Ocean University)

  • Xianghui Zhang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Xiang Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center
    BGI Research)

  • Yifang Lu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Hang He

    (BGI Research
    BGI Research)

  • Yubang Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Hongxi Chen

    (BGI Research
    BGI Research)

  • Qun Liu

    (BGI Research
    BGI Research)

  • Yingyi Huang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Zhao Jia

    (Shanghai Ocean University)

  • Shuo Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Yangqing Zhang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Shenglei Han

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Shuhong Jiang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Mingming Yang

    (BGI Research
    BGI Research)

  • Yingying Zhang

    (BGI Research
    BGI Research)

  • Li Zhou

    (BGI Research
    BGI Research)

  • Fujian Tan

    (BGI Research
    BGI Research)

  • Qianyue Ji

    (MGI Tech)

  • Liang Meng

    (BGI Research
    BGI Research)

  • Rui Wang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Yuyan Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Kaiqiang Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Qian Wang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Inge Seim

    (Nanjing Normal University
    Queensland University of Technology)

  • Jun Zou

    (Shanghai Ocean University)

  • Guangyi Fan

    (BGI Research
    BGI Research
    BGI Research)

  • Shanshan Liu

    (MGI Tech)

  • Changwei Shao

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

Abstract

Elucidating cellular architecture and cell-type evolution across species is central to understanding immune system function and susceptibility to disease. Adaptive immunity is a shared trait of the common ancestor of cartilaginous and bony fishes. However, evolutionary features of lymphocytes in these two jawed vertebrates remain unclear. Here, we present a single-cell RNA sequencing atlas of immune cells from cartilaginous (white-spotted bamboo shark) and bony (zebrafish and Chinese tongue sole) fishes. Cross-species comparisons show that the same cell types across different species exhibit similar transcriptional profiles. In the bamboo shark, we identify a phagocytic B cell population expressing several pattern recognition receptors, as well as a T cell sub-cluster co-expressing both T and B cell markers. In contrast to a division by function in the bony fishes, we show close linkage and poor functional specialization among lymphocytes in the cartilaginous fish. Our cross-species single-cell comparison presents a resource for uncovering the origin and evolution of the gnathostome immune system.

Suggested Citation

  • Hong-Yan Wang & Jian-Yang Chen & Yanan Li & Xianghui Zhang & Xiang Liu & Yifang Lu & Hang He & Yubang Li & Hongxi Chen & Qun Liu & Yingyi Huang & Zhao Jia & Shuo Li & Yangqing Zhang & Shenglei Han & S, 2024. "Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51761-4
    DOI: 10.1038/s41467-024-51761-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51761-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51761-4?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. Bastiaan Star & Alexander J. Nederbragt & Sissel Jentoft & Unni Grimholt & Martin Malmstrøm & Tone F. Gregers & Trine B. Rounge & Jonas Paulsen & Monica H. Solbakken & Animesh Sharma & Ola F. Wetten &, 2011. "The genome sequence of Atlantic cod reveals a unique immune system," Nature, Nature, vol. 477(7363), pages 207-210, September.
    2. Rebecca D. Hodge & Trygve E. Bakken & Jeremy A. Miller & Kimberly A. Smith & Eliza R. Barkan & Lucas T. Graybuck & Jennie L. Close & Brian Long & Nelson Johansen & Osnat Penn & Zizhen Yao & Jeroen Egg, 2019. "Conserved cell types with divergent features in human versus mouse cortex," Nature, Nature, vol. 573(7772), pages 61-68, September.
    3. Byrappa Venkatesh & Alison P. Lee & Vydianathan Ravi & Ashish K. Maurya & Michelle M. Lian & Jeremy B. Swann & Yuko Ohta & Martin F. Flajnik & Yoichi Sutoh & Masanori Kasahara & Shawn Hoon & Vamshidha, 2014. "Elephant shark genome provides unique insights into gnathostome evolution," Nature, Nature, vol. 505(7482), pages 174-179, January.
    4. Byrappa Venkatesh & Alison P. Lee & Vydianathan Ravi & Ashish K. Maurya & Michelle M. Lian & Jeremy B. Swann & Yuko Ohta & Martin F. Flajnik & Yoichi Sutoh & Masanori Kasahara & Shawn Hoon & Vamshidha, 2014. "Correction: Corrigendum: Elephant shark genome provides unique insights into gnathostome evolution," Nature, Nature, vol. 513(7519), pages 574-574, September.
    5. Tzachi Hagai & Xi Chen & Ricardo J. Miragaia & Raghd Rostom & Tomás Gomes & Natalia Kunowska & Johan Henriksson & Jong-Eun Park & Valentina Proserpio & Giacomo Donati & Lara Bossini-Castillo & Felipe , 2018. "Gene expression variability across cells and species shapes innate immunity," Nature, Nature, vol. 563(7730), pages 197-202, November.
    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. Yuuki Y. Watanabe & Nicholas L. Payne, 2023. "Thermal sensitivity of metabolic rate mirrors biogeographic differences between teleosts and elasmobranchs," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    2. Anthony K. Redmond & Dearbhaile Casey & Manu Kumar Gundappa & Daniel J. Macqueen & Aoife McLysaght, 2023. "Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Shan Nan Chen & Zhen Gan & Jing Hou & Yue Cong Yang & Lin Huang & Bei Huang & Su Wang & Pin Nie, 2022. "Identification and establishment of type IV interferon and the characterization of interferon-υ including its class II cytokine receptors IFN-υR1 and IL-10R2," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Yuzhou Chang & Jixin Liu & Yi Jiang & Anjun Ma & Yao Yu Yeo & Qi Guo & Megan McNutt & Jordan E. Krull & Scott J. Rodig & Dan H. Barouch & Garry P. Nolan & Dong Xu & Sizun Jiang & Zihai Li & Bingqiang , 2024. "Graph Fourier transform for spatial omics representation and analyses of complex organs," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    5. Nelson Johansen & Hongru Hu & Gerald Quon, 2023. "Projecting RNA measurements onto single cell atlases to extract cell type-specific expression profiles using scProjection," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    8. Roy Oelen & Dylan H. Vries & Harm Brugge & M. Grace Gordon & Martijn Vochteloo & Chun J. Ye & Harm-Jan Westra & Lude Franke & Monique G. P. Wijst, 2022. "Single-cell RNA-sequencing of peripheral blood mononuclear cells reveals widespread, context-specific gene expression regulation upon pathogenic exposure," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Daniel J. Lodge & Hannah B. Elam & Angela M. Boley & Jennifer J. Donegan, 2023. "Discrete hippocampal projections are differentially regulated by parvalbumin and somatostatin interneurons," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Zhiyuan Yuan & Yisi Li & Minglei Shi & Fan Yang & Juntao Gao & Jianhua Yao & Michael Q. Zhang, 2022. "SOTIP is a versatile method for microenvironment modeling with spatial omics data," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Biao Zhang & Shuqin Zhang & Shihua Zhang, 2024. "Whole brain alignment of spatial transcriptomics between humans and mice with BrainAlign," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Jiao Qu & Fa Yang & Tao Zhu & Yingshuo Wang & Wen Fang & Yan Ding & Xue Zhao & Xianjia Qi & Qiangmin Xie & Ming Chen & Qiang Xu & Yicheng Xie & Yang Sun & Dijun Chen, 2022. "A reference single-cell regulomic and transcriptomic map of cynomolgus monkeys," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Malosree Maitra & Haruka Mitsuhashi & Reza Rahimian & Anjali Chawla & Jennie Yang & Laura M. Fiori & Maria Antonietta Davoli & Kelly Perlman & Zahia Aouabed & Deborah C. Mash & Matthew Suderman & Nagu, 2023. "Cell type specific transcriptomic differences in depression show similar patterns between males and females but implicate distinct cell types and genes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Stan L. W. Driessens & Anna A. Galakhova & Djai B. Heyer & Isabel J. Pieterse & René Wilbers & Eline J. Mertens & Femke Waleboer & Tim S. Heistek & Loet Coenen & Julia R. Meijer & Sander Idema & Phili, 2023. "Genes associated with cognitive ability and HAR show overlapping expression patterns in human cortical neuron types," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Orshay Gabay & Yoav Shoshan & Eli Kopel & Udi Ben-Zvi & Tomer D. Mann & Noam Bressler & Roni Cohen‐Fultheim & Amos A. Schaffer & Shalom Hillel Roth & Ziv Tzur & Erez Y. Levanon & Eli Eisenberg, 2022. "Landscape of adenosine-to-inosine RNA recoding across human tissues," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Eunnyung Bae & Ping Huang & Gaёlle Müller-Greven & Dolores Hambardzumyan & Andrew Edward Sloan & Amy S. Nowacki & Nicholas Marko & Cathleen R. Carlin & Candece L. Gladson, 2022. "Integrin α3β1 promotes vessel formation of glioblastoma-associated endothelial cells through calcium-mediated macropinocytosis and lysosomal exocytosis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Hao Xu & Shuyan Wang & Minghao Fang & Songwen Luo & Chunpeng Chen & Siyuan Wan & Rirui Wang & Meifang Tang & Tian Xue & Bin Li & Jun Lin & Kun Qu, 2023. "SPACEL: deep learning-based characterization of spatial transcriptome architectures," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. Jingyang Qian & Jie Liao & Ziqi Liu & Ying Chi & Yin Fang & Yanrong Zheng & Xin Shao & Bingqi Liu & Yongjin Cui & Wenbo Guo & Yining Hu & Hudong Bao & Penghui Yang & Qian Chen & Mingxiao Li & Bing Zha, 2023. "Reconstruction of the cell pseudo-space from single-cell RNA sequencing data with scSpace," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    19. Ying Lei & Mengnan Cheng & Zihao Li & Zhenkun Zhuang & Liang Wu & Yunong sun & Lei Han & Zhihao Huang & Yuzhou Wang & Zifei Wang & Liqin Xu & Yue Yuan & Shang Liu & Taotao Pan & Jiarui Xie & Chuanyu L, 2022. "Spatially resolved gene regulatory and disease-related vulnerability map of the adult Macaque cortex," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    20. Yueqi Wang & Simone Chiola & Guang Yang & Chad Russell & Celeste J. Armstrong & Yuanyuan Wu & Jay Spampanato & Paisley Tarboton & H. M. Arif Ullah & Nicolas U. Edgar & Amelia N. Chang & David A. Harmi, 2022. "Modeling human telencephalic development and autism-associated SHANK3 deficiency using organoids generated from single neural rosettes," Nature Communications, Nature, vol. 13(1), pages 1-25, 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_s41467-024-51761-4. 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.