Skip to main content
SpringerLink
Log in

Aeromonas hydrophila can modulate synchronization of immune response in gut-liver axis of red crucian carp via the breach of gut barrier

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

The survival of farmed fish can be threatened by incidence of Aeromonas hydrophila infection. In addition, gut infection may promote dysbiosis of gut flora and dysregulate immune response in gut-liver axis in teleost fish. The current study aimed to evaluate the pathogenesis of A. hydrophila on gut barrier breach and synchronized immune response in gut-liver axis of RCCs. RCCs were subjected to continuous anal-intubation with A. hydrophila. Midgut sections were stained with periodic acid-Schiff (PAS) and immune-related gene expressions and biochemical indices in gut-liver axis were investigated. The severe midgut injury was detected in RCC anal-intubated with A. hydrophila, along with atrophy of the midgut villi, and the expression levels of tight junction (TJ) genes were consistently lower than those of the control (P < 0.05). Moreover, RCC receiving anal intubation with A. hydrophila showed the upregulation of pathological indices and immure genes in the midgut and liver. These findings demonstrated that gut infection with A. hydrophila can significantly disrupt epithelial permeability to exacerbate gut barrier breach and increase bacterial burdens in tissues as well as dysregulate immune response in gut-liver axis of RCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The authors confirm that the data supporting the findings of this study are available within the article [and/or] its supplementary materials.

References

  • Abd-El-Malek AM (2017) Incidence and virulence characteristics of Aeromonas spp. in fish. Veterinary world 10:34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albillos A, De Gottardi A, Rescigno M (2020) The gut-liver axis in liver disease: pathophysiological basis for therapy. Journal of hepatology 72:558–577

    Article  CAS  PubMed  Google Scholar 

  • Anturaniemi J, Zaldívar-López S, Savelkoul HF, Elo K, Hielm-Björkman A (2020) The effect of atopic dermatitis and diet on the skin transcriptome in Staffordshire Bull Terriers. Frontiers in Veterinary Science:763

  • Atli G, Ariyurek SY, Kanak EG, Canli M (2015) Alterations in the serum biomarkers belonging to different metabolic systems of fish (Oreochromis niloticus) after Cd and Pb exposures. Environmental Toxicology and Pharmacology 40:508–515

    Article  CAS  PubMed  Google Scholar 

  • Austin B (1998) The effects of pollution on fish health. Journal of applied microbiology 85:234S–242S

    Article  PubMed  Google Scholar 

  • Awan F, Dong Y, Wang N, Liu J, Ma K, Liu Y (2018) The fight for invincibility: environmental stress response mechanisms and Aeromonas hydrophila. Microbial pathogenesis 116:135–145

    Article  PubMed  Google Scholar 

  • Barrera-Chimal J, Pérez-Villalva R, Ortega JA, Uribe N, Gamba G, Cortés-González C et al (2014) Intra-renal transfection of heat shock protein 90 alpha or beta (Hsp90α or Hsp90β) protects against ischemia/reperfusion injury. Nephrology Dialysis Transplantation 29:301–312

    Article  CAS  Google Scholar 

  • Dee CT, Nagaraju RT, Athanasiadis EI, Gray C, Fernandez del Ama L, Johnston SA et al (2016) CD4-transgenic zebrafish reveal tissue-resident Th2-and regulatory T cell–like populations and diverse mononuclear phagocytes. The Journal of Immunology 197:3520–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Zhang Y, Chen H, Xu L, Wang Q, Feng J (2020) Gut–liver immune response and gut microbiota profiling reveal the pathogenic mechanisms of Vibrio harveyi in pearl gentian grouper (Epinephelus lanceolatus♂× E. fuscoguttatus♀). Frontiers in immunology 11:607754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong K, Chen W, Pan X, Wang H, Sun Y, Qian C et al (2022) FCER1G positively relates to macrophage infiltration in clear cell renal cell carcinoma and contributes to unfavorable prognosis by regulating tumor immunity. BMC cancer 22:1–20

    Article  CAS  Google Scholar 

  • Gao B, Jeong WI, Tian Z (2008) Liver: an organ with predominant innate immunity. Hepatology 47:729–736

    Article  CAS  PubMed  Google Scholar 

  • Gray S, Stickler D, Bryant T (1990) The incidence of virulence factors in mesophilic Aeromonas species isolated from farm animals and their environment. Epidemiology & Infection 105:277–294

    Article  CAS  Google Scholar 

  • Holland MCH, Lambris JD (2002) The complement system in teleosts. Fish & Shellfish Immunology 12:399–420

    Article  CAS  Google Scholar 

  • Jeong MK, Kim B-H (2022) Grading criteria of histopathological evaluation in BCOP assay by various staining methods. Toxicological Research 38:9–17

    Article  MathSciNet  CAS  PubMed  Google Scholar 

  • Kagnoff MF, Eckmann L (1997) Epithelial cells as sensors for microbial infection. The Journal of clinical investigation 100:6–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Current gastroenterology reports 12:319–330

    Article  PubMed  PubMed Central  Google Scholar 

  • Kümmerer K (2004) Resistance in the environment. Journal of antimicrobial chemotherapy 54:311–320

    Article  PubMed  Google Scholar 

  • Li Z, Wang ZW, Wang Y, Gui JF (2018) Crucian carp and gibel carp culture. Aquaculture in China: success stories and modern 25:149–157

    Article  Google Scholar 

  • Luo S-W, Wei W, Yang P, Lai C-M, Liang QJ, Liu Y et al (2019) Characterization of a CD59 in orange-spotted grouper (Epinephelus coioides). Fish & shellfish immunology 89:486–497

    Article  CAS  Google Scholar 

  • Ma X, Wang Y, Yin H, Hua L, Zhang X, Xiao J et al (2021) Down-regulated long non-coding RNA RMST ameliorates dopaminergic neuron damage in Parkinson’s disease rats via regulation of TLR/NF-κB signaling pathway. Brain research bulletin 174:22–30

    Article  CAS  PubMed  Google Scholar 

  • Morrish E, Ruland J (2022) Cytotoxic FCER1G+ innate-like T cells: new potential for tumour immunotherapy. Signal Transduction and Targeted Therapy 7:204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nielsen ME, Høi L, Schmidt A, Qian D, Shimada T, Shen J, Larsen J (2001) Is Aeromonas hydrophila the dominant motile Aeromonas species that causes disease outbreaks in aquaculture production in the Zhejiang Province of China? Diseases of aquatic organisms 46:23–29

    Article  CAS  PubMed  Google Scholar 

  • Oliveira ST, Veneroni-Gouveia G, Costa MM (2012) Molecular characterization of virulence factors in Aeromonas hydrophila obtained from fish. Pesquisa Veterinária Brasileira 32:701–706

    Article  Google Scholar 

  • Portoles P, Rojo J, Golby A, Bonneville M, Gromkowski S, Greenbaum L et al (1989) Monoclonal antibodies to murine CD3 epsilon define distinct epitopes, one of which may interact with CD4 during T cell activation. Journal of immunology 142:4169–4175

    Article  CAS  Google Scholar 

  • Qi Z-H, Liu Y-F, Luo S-W, Chen C-X, Liu Y, Wang W-N (2013) Molecular cloning, characterization and expression analysis of tumor suppressor protein p53 from orange-spotted grouper, Epinephelus coioides in response to temperature stress. Fish & shellfish immunology 35:1466–1476

    Article  CAS  Google Scholar 

  • Rizwan S, ReddySekhar P, MalikAsrar B (2014) Reactive oxygen species in inflammation and tissue injury. Antioxidants & redox signaling

  • Rodger HD (2016) Fish disease causing economic impact in global aquaculture. Fish vaccines:1–34

  • Schäfer H, Mathey D, Hugo F, Bhakdi S (1986) Deposition of the terminal C5b-9 complement complex in infarcted areas of human myocardium. The Journal of Immunology 137:1945–1949

    Article  PubMed  Google Scholar 

  • Schneeberger EE, Lynch RD (2004) The tight junction: a multifunctional complex. American Journal of Physiology-Cell Physiology 286:C1213–C1228

    Article  CAS  PubMed  Google Scholar 

  • Shan Y, Zhang Y, Zhuo X, Li X, Peng J, Fang W (2016) Matrix metalloproteinase-9 plays a role in protecting zebrafish from lethal infection with Listeria monocytogenes by enhancing macrophage migration. Fish & shellfish immunology 54:179–187

    Article  CAS  Google Scholar 

  • Song X, Zhao J, Bo Y, Liu Z, Wu K, Gong C (2014) Aeromonas hydrophila induces intestinal inflammation in grass carp (Ctenopharyngodon idella): an experimental model. Aquaculture 434:171–178

    Article  Google Scholar 

  • Tlaskalová-Hogenová H, Štěpánková R, Kozáková H, Hudcovic T, Vannucci L, Tučková L et al (2011) The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cellular & molecular immunology 8:110–120

    Article  Google Scholar 

  • Uribe C, Folch H, Enríquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Veterinarni Medicina 56:486

    Article  CAS  Google Scholar 

  • Wang L, Fan C, Xu W, Zhang Y, Dong Z, Xiang J et al (2017) Characterization and functional analysis of a novel C1q-domain-containing protein in Japanese flounder (Paralichthys olivaceus). Developmental & Comparative Immunology 67:322–332

    Article  CAS  Google Scholar 

  • Warner K, Hamza M, Oliver-Smith A, Renaud F, Julca A (2010) Climate change, environmental degradation and migration. Natural Hazards 55:689–715

    Article  Google Scholar 

  • Wischhusen P, Larroquet L, Durand T, Oger C, Galano J-M, Rocher A et al (2020) Oxidative stress and antioxidant response in rainbow trout fry exposed to acute hypoxia is affected by selenium nutrition of parents and during first exogenous feeding. Free Radical Biology and Medicine 155:99–113

    Article  CAS  PubMed  Google Scholar 

  • Wu N, Song Y-L, Wang B, Zhang X-Y, Zhang X-J, Wang Y-L et al (2016) Fish gut-liver immunity during homeostasis or inflammation revealed by integrative transcriptome and proteome studies. Scientific reports 6:1–17

    Google Scholar 

  • Xiong N-X, Fang Z-X, Kuang X-Y, Ou J, Luo S-W, Liu S-J (2023) Integrated analysis of gene expressions and metabolite features unravel immunometabolic interplay in hybrid fish (Carassius cuvieri♀× Carassius auratus red var♂) infected with Aeromonas hydrophila. Aquaculture 563:738981

    Article  Google Scholar 

  • Xiong N-X, Luo S-W, Fan L-F, Mao Z-W, Luo K-K, Liu S-J et al (2021) Comparative analysis of erythrocyte hemolysis, plasma parameters and metabolic features in red crucian carp (Carassius auratus red var) and triploid hybrid fish following Aeromonas hydrophila challenge. Fish & Shellfish Immunology 118:369–384

    Article  CAS  Google Scholar 

  • Xiong N-X, Mao Z-W, Ou J, Fan L-F, Chen Y, Luo S-W et al (2022a) Metabolite features and oxidative response in kidney of red crucian carp (Carassius auratus red var) after Aeromonas hydrophila challenge. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 255:109293

    CAS  Google Scholar 

  • Xiong N-X, Ou J, Fan L-F, Kuang X-Y, Fang Z-X, Luo S-W et al (2022b) Blood cell characterization and transcriptome analysis reveal distinct immune response and host resistance of different ploidy cyprinid fish following Aeromonas hydrophila infection. Fish & Shellfish Immunology 120:547–559

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the National Natural Science Foundation of China, China (grant no. 31902363), Hunan Provincial Natural Science Foundation of China, China (grant no.2021JJ40340).

Author information

Authors and Affiliations

  1. State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, 410081, People’s Republic of China

    Fei Wang, Zi-Le Qin, Wei-Sheng Luo, Ning-Xia Xiong & Sheng-Wei Luo

Authors
  1. Fei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zi-Le Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei-Sheng Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ning-Xia Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sheng-Wei Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Fei Wang performed methodology and formal analysis. Zi-Le Qin and Wei-Sheng Luo performed methodology. Ning-Xia Xiong performed formal analysis and verification. Sheng-Wei Luo performed Conceptualization, supervision, project management and article writing.

The authors of this manuscript are all aware of the journal to which the manuscript was submitted, and all agree to continue to support the follow-up work.

Corresponding author

Correspondence to Sheng-Wei Luo.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the case and use of animals were followed. Chinese animal welfare laws, guidelines and policies (GB/T 35892-2018).

Competing interests

The authors declare no competing of interests.

Additional information

Handling Editor: Patrice Forget

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

1. Severe tissue injury and GC hyperplasia was monitored in the midgut of A. hydrophila-perfused RCC.

2. RCC receiving gut infection with A. hydrophila showed a sharp decreased level of tight junction genes.

3. Increased bacterial burdens in tissues and altered immune response were monitored in gut-liver axis of RCC after continuous gut infection.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, F., Qin, ZL., Luo, WS. et al. Aeromonas hydrophila can modulate synchronization of immune response in gut-liver axis of red crucian carp via the breach of gut barrier. Aquacult Int 32, 871–885 (2024). https://doi.org/10.1007/s10499-023-01185-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-023-01185-6

Keywords

Search

Navigation