Integrated time-series biochemical, transcriptomic, and metabolomic analyses reveal key metabolites and signaling pathways in the liver of the Chinese soft-shelled turtle (Pelodiscus sinensis) against Aeromonas hydrophila infection

Front Immunol. 2024 May 10:15:1376860. doi: 10.3389/fimmu.2024.1376860. eCollection 2024.

Abstract

Introduction: Aeromonas hydrophila, a bacterium widely distributed in the natural environment, causes multiple diseases in various animals. Exploring the mechanism of the host defense against A. hydrophila can help develop efficient strategies against Aeromonas infection.

Methods: Herein, we investigated the temporal influence of A. hydrophila on the Chinese soft-shelled turtle, an economically important species, at the biochemical, transcriptomic, and metabolomic levels. Plasma parameters were detected with the test kits. Transcriptome and metabolome were respectively applied to screen the differentially expressed genes and metabolites.

Results: The contents or activities of these plasma parameters were significantly increased at 24 hpi and declined at 96 hpi, indicating that 24 and 96 hpi were two important time points during infection. Totals of 3121 and 274 differentially expressed genes (DEGs) from the transcriptome while 74 and 91 differentially abundant metabolites (DAMs) from the metabolome were detected at 24 and 96 hpi. The top DEGs at 24 hpi included Ccl2, Ccl3, Ccl4, Il1β, Il6, Il7, Il15, Tnf, and Tnfr1 while Zap70, Cd3g, Cd8a, Itk, Pik3r3, Cd247, Malt1, and Cd4 were the most abundant at 96 hpi. The predominant DAMs included O-phospho-L-serine, γ-Aminobutyric acid, orotate, L-tyrosine, and L-tryptophan at 24 hpi, as well as L-glutamic acid, L-arginine, glutathione, glutathione disulfide, and citric acid at 96 hpi.

Discussion: The combined analysis of DEGs and DAMs revealed that tryptophan metabolism, nicotinate and nicotinamide metabolism, as well as starch and sucrose metabolism, were the most important signaling pathways at the early infective stage while tyrosine metabolism, pyrimidine metabolism, as well as alanine, aspartate and glutamate metabolism were the most crucial pathways at the later stage. In general, our results indicated that the Chinese soft-shelled turtle displays stage-specific physiological responses to resist A. hydrophila infection.

Keywords: Aeromonas hydrophila; Chinese soft-shelled turtle; liver; metabolome; plasma parameters; transcriptome.

MeSH terms

  • Aeromonas hydrophila* / physiology
  • Animals
  • Gene Expression Profiling
  • Gram-Negative Bacterial Infections* / immunology
  • Gram-Negative Bacterial Infections* / veterinary
  • Liver* / metabolism
  • Metabolome*
  • Metabolomics*
  • Signal Transduction*
  • Transcriptome*
  • Turtles* / genetics
  • Turtles* / immunology
  • Turtles* / microbiology

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The work was supported by the National Natural Science Foundation of China (32302981, 3220210604, and 32102792); the Central Public-Interest Scientific Institution Basal Research Fund (2023SJHX1); the Key Laboratory of Environment Controlled Aquaculture (Dalian Ocean University, 202310); the Key Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs (20220203); the Selection Breeding of the High-Quality Fast-Growing Chinese Soft-Shelled Turtle and Studies on Efficient and Healthy Farming Technology (2022-SPY-00-015); the Construction of a DNA Molecular Fingerprinting Library for the Germplasm Resources of the Grass Carp and the Chinese Soft-Shelled Turtle (2022-SJS-00-001); the Central Public-Interest Scientific Institution Basal Research Fund (2023TD38); and the China-ASEAN Maritime Cooperation Fund (CAMC-2018F).