Single-cell RNA sequencing analysis of shrimp immune cells identifies macrophage-like phagocytes

  1. Peng Yang
  2. Yaohui Chen
  3. Zhiqi Huang
  4. Huidan Xia
  5. Ling Cheng
  6. Hao Wu
  7. Yueling Zhang
  8. Fan Wang  Is a corresponding author
  1. Shantou University, China
  2. Genedenovo Biotechnology Company Limited, China

Abstract

Despite the importance of innate immunity in invertebrates, the diversity and function of innate immune cells in invertebrates are largely unknown. Using single-cell RNA-seq, we identified prohemocytes, monocytic hemocytes, and granulocytes as the three major cell-types in the white shrimp hemolymph. Our results identified a novel macrophage-like subset called monocytic hemocytes 2 (MH2) defined by the expression of certain marker genes, including Nlrp3 and Casp1. This subtype of shrimp hemocytes is phagocytic and expresses markers that indicate some conservation with mammalian macrophages. Combined, our work resolves the heterogenicity of hemocytes in a very economically important aquatic species and identifies a novel innate immune cell subset that is likely a critical player in the immune responses of shrimp to threatening infectious diseases affecting this industry.

Data availability

The sequence data reported in this paper have been deposited in the Genome Sequence Archive of the Beijing Institute of Genomics, Chinese Academy of Sciences, gsa.big.ac.cn (accession no. PRJCA006297). All other data are available in this manuscript and online in the Supplementary Material.

The following data sets were generated

Article and author information

Author details

  1. Peng Yang

    Institute of Marine Sciences, Shantou University, Shantou, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8298-8926
  2. Yaohui Chen

    Department of Biology, Shantou University, Shantou, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4044-4373
  3. Zhiqi Huang

    Department of Biology, Shantou University, Shantou, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Huidan Xia

    Department of Biology, Shantou University, Shantou, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ling Cheng

    Genedenovo Biotechnology Company Limited, Guangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Hao Wu

    Genedenovo Biotechnology Company Limited, Guangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yueling Zhang

    Institute of Marine Sciences, Shantou University, Shantou, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Fan Wang

    Institute of Marine Sciences, Shantou University, Shantou, China
    For correspondence
    wangfan@stu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6059-6956

Funding

National Natural Science Foundation of China (41976123)

  • Fan Wang

Guangdong Science and Technology Department (14600703)

  • Fan Wang

Li Ka Shing Foundation (2020LKSFG01E)

  • Yueling Zhang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All the animal-related experiments were in accordance with Shantou University guidelines.

Copyright

© 2022, Yang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,553
    views
  • 589
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Peng Yang
  2. Yaohui Chen
  3. Zhiqi Huang
  4. Huidan Xia
  5. Ling Cheng
  6. Hao Wu
  7. Yueling Zhang
  8. Fan Wang
(2022)
Single-cell RNA sequencing analysis of shrimp immune cells identifies macrophage-like phagocytes
eLife 11:e80127.
https://doi.org/10.7554/eLife.80127

Share this article

https://doi.org/10.7554/eLife.80127

Further reading

    1. Immunology and Inflammation
    Arijit Chakraborty, Arunava Bandyopadhaya ... Laurence G Rahme
    Research Article

    How bacterial pathogens exploit host metabolism to promote immune tolerance and persist in infected hosts remains elusive. To achieve this, we show that Pseudomonas aeruginosa (PA), a recalcitrant pathogen, utilizes the quorum sensing (QS) signal 2’-aminoacetophenone (2-AA). Here, we unveil how 2-AA-driven immune tolerization causes distinct metabolic perturbations in murine macrophages’ mitochondrial respiration and bioenergetics. We present evidence indicating that these effects stem from decreased pyruvate transport into mitochondria. This reduction is attributed to decreased expression of the mitochondrial pyruvate carrier (Mpc1), which is mediated by diminished expression and nuclear presence of its transcriptional regulator, estrogen-related nuclear receptor alpha (Esrra). Consequently, Esrra exhibits weakened binding to the Mpc1 promoter. This outcome arises from the impaired interaction between Esrra and the peroxisome proliferator-activated receptor gamma coactivator 1-alpha (Ppargc1a). Ultimately, this cascade results in diminished pyruvate influx into mitochondria and, consequently reduced ATP production in tolerized murine and human macrophages. Exogenously added ATP in infected macrophages restores the transcript levels of Mpc1 and Esrra and enhances cytokine production and intracellular bacterial clearance. Consistent with the in vitro findings, murine infection studies corroborate the 2-AA-mediated long-lasting decrease in ATP and acetyl-CoA and its association with PA persistence, further supporting this QS signaling molecule as the culprit of the host bioenergetic alterations and PA persistence. These findings unveil 2-AA as a modulator of cellular immunometabolism and reveal an unprecedented mechanism of host tolerance to infection involving the Ppargc1a/Esrra axis in its influence on Mpc1/OXPHOS-dependent energy production and PA clearance. These paradigmatic findings pave the way for developing treatments to bolster host resilience to pathogen-induced damage. Given that QS is a common characteristic of prokaryotes, it is likely that 2-AA-like molecules with similar functions may be present in other pathogens.

    1. Immunology and Inflammation
    Alessandra Machado Araujo, Joseph D Dekker ... Haley O Tucker
    Research Article

    We identified a novel mouse plasmacytoid dendritic cell (pDC) lineage derived from the common lymphoid progenitors (CLPs) that is dependent on expression of Bcl11a. These CLP-derived pDCs, which we refer to as ‘B-pDCs’, have a unique gene expression profile that includes hallmark B cell genes, normally not expressed in conventional pDCs. Despite expressing most classical pDC markers such as SIGLEC-H and PDCA1, B-pDCs lack IFN-α secretion, exhibiting a distinct inflammatory profile. Functionally, B-pDCs induce T cell proliferation more robustly than canonical pDCs following Toll-like receptor 9 (TLR9) engagement. B-pDCs, along with another homogeneous subpopulation of myeloid-derived pDCs, display elevated levels of the cell surface receptor tyrosine kinase AXL, mirroring human AXL+ transitional DCs in function and transcriptional profile. Murine B-pDCs therefore represent a phenotypically and functionally distinct CLP-derived DC lineage specialized in T cell activation and previously not described in mice.