Single-cell transcriptome analysis reveals a cellular immune response in freshwater dark sleeper (Odontobutis potamophila) after infection with Aeromonas veronii

Guoxing Liu; Chenxi Zhu; Xiaojian Gao; You Zheng; Xinhai Zhu; Hucheng Jiang; Wanhong Wei; Qichen Jiang; Xiaojun Zhang

doi:10.3389/fphys.2023.1201914

Single-cell transcriptome analysis reveals a cellular immune response in freshwater dark sleeper (Odontobutis potamophila) after infection with Aeromonas veronii

Front Physiol. 2023 May 18:14:1201914. doi: 10.3389/fphys.2023.1201914. eCollection 2023.

Authors

Guoxing Liu^{1

2

3}, Chenxi Zhu², Xiaojian Gao¹, You Zheng^{2

3}, Xinhai Zhu¹, Hucheng Jiang^{2

3}, Wanhong Wei¹, Qichen Jiang^{1

2

3}, Xiaojun Zhang¹

Affiliations

¹ College of Animal Science and Technology, Yangzhou University, Yangzhou, China.
² Freshwater Fisheries Research Institute of Jiangsu Province, Nanjing, China.
³ Low-temperature Germplasm Bank of Important Economic Fish (Freshwater Fisheries Research Institute of Jiangsu Province) of Jiangsu Provincial Science and Technology Resources (Agricultural Germplasm Resources) Coordination Service Platform, Nanjing, China.

Abstract

The bacterium Aeromonas veronii is a co-pathogenic species that can negatively impact the health of both humans and aquatic animals. In this study, we used single-cell transcriptome analysis (scRNA-seq) to investigate the effects of infection with A. veronii on head kidney cells and the regulation of gene expression in the dark sleeper (Odontobutis potamophila). scRNA-seq was used to assess the effects of infection with A. veronii in O. potamophila B cells, endothelial cells, macrophages, and granulocytes, and differential enrichment analysis of gene expression in B cells and granulocytes was performed. The analyses revealed a significant increase in neutrophils and decrease in eosinophils in granulocytes infected with A. veronii. Activation of neutrophils enhanced ribosome biogenesis by up-regulating the expression of RPS12 and RPL12 to fight against invading pathogens. Crucial pro-inflammatory mediators IL1B, IGHV1-4, and the major histocompatibility class II genes MHC2A and MHC2DAB, which are involved in virulence processes, were upregulated, suggesting that A. veronii activates an immune response that presents antigens and activates immunoglobulin receptors in B cells. These cellular immune responses triggered by infection with A. veronii enriched the available scRNA-seq data for teleosts, and these results are important for understanding the evolution of cellular immune defense and functional differentiation of head kidney cells.

Keywords: Aeromonas veronii; B cell; Odontobutis potamophila; ScRNA-seq; granulocytes; immune response.

Grants and funding

This work was supported by the earmarked fund for Jiangsu Agricultural Industry Technology System (JATS (2022) 415; JATS (2022) 417) and the Agricultural Major New Variety Creation Project in Jiangsu province (PZCZ201743).