Skip to main content
Log in

Transcriptome analysis of the immunoprotective effect of Bacillus licheniformis on the intestinal tract of Carassius auratus gibelio infected with Aeromonas hydrophila

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Carassius auratus gibelio, commonly known as crucian carp, is the main species of freshwater aquaculture in China. Due to high-density aquaculture and environmental pollution, various diseases continue to emerge, especially the diseases caused by pathogenic bacteria have seriously restricted the development of freshwater aquaculture. Among these, Aeromonas hydrophila (AH) is the one of the most serious fish disease causing economic losses among fish farmers. An in-depth understanding of the crucian carp’s immune system and its genes involved in the response to bacterial infection is necessary for disease control. In this study, the breeding period was divided into the control group (C group) and the Bacillus licheniformis (B. licheniformis) group (BL group). After 4 weeks of culture, the crucian carp was infected with AH and divided into the control group (Cg group) and the B. licheniformis group (BLg group). After the 72-h challenge, the Illumina-based paired-end sequencing approach to analyze the transcriptome profile of the crucian carp gut following AH infection. A total of 472.05 million valid reads were found from the four intestinal samples and 403.18 million reads were mapped successfully, of which 243.34 million were unique. About GO enrichment analysis, significant differentially expressed genes (DEGs) were more in biological process (406 DEGs), regulation of transcription, DNA-templated (345 DEGs), and signal transduction (304 DEGs). In the cell components, membrane (1913 DEGs) and integral component of membrane (1789 DEGs) had a higher number of significantly different genes. In the molecular function, metal ion binding (780 DEGs), ATP binding (535 DEGs), transferase activity (491 DEGs), and nucleotide binding (482 DEGs) have a large number of significantly different genes. Regarding the KEGG enrich analysis section, this study is arranged in ascending P-value order, andthe most significant signaling paths are lysosome, glucose metabolism, cycline cycline receiver interaction, and phagosome. Among them, the cycline cycline receiver interaction has the highest difference in significant genes. In addition, 5 immune-related genes were selected for real-time fluorescence quantitative PCR analysis to verify the RNA-seq data, and the results showed that the expression of all 5 genes was upregulated, which was consistent with the results of our RNA-seq analysis. After analysis, it was found that B. licheniformis can alleviate the inflammatory response and protect the fish body. Our results provide a reference for further analysis of the antagonism and mitigation mechanism of B. licheniformis against AH.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

Not applicable.

References

  • Camino OM, Castro R, Dixon B et al (2012) Identification of a novel CCR7 gene in rainbow trout with differential expression in the context of mucosal or systemic infection. Dev Comp Immunol 38(2):302–311

    Google Scholar 

  • Castro R, Bromage E, Abos B et al (2014) CCR7 is mainly expressed in teleost gills, where it defines an IgD+IgM- B lymphocyte subset. J Immunol 192(3):1257–1266

    CAS  PubMed  Google Scholar 

  • Chandrakala AN, Sukul D et al (2012) Induction of brain natriuretic peptide and monocyte chemotactic protein-1 gene expression by oxidized low-density lipoprotein: relevance to ischemic heart failure. Am J Physiol 302:165–177

    Google Scholar 

  • Chen B, Peng M, Tong W et al (2020) The quorum quenching bacterium Bacillus licheniformis T-1 protects zebrafish against Aeromonas hydrophila infection. Prob Antimicrob Proteins 1:12

    Google Scholar 

  • Chi C, Liu JY, Fei SZ et al (2014) Effect of intestinal autochthonous probiotics isolated from the gut of sea cucumber (Apostichopus japonicus) on immune response and growth of A japonicus. Fish Shell Immunol 38(2):367–373

    CAS  Google Scholar 

  • Cui Y (2021) Effects of hyperbaric oxygen therapy on serum levels of interleukin-1β, interleukin-2, interleukin-8, tumor necrosis factor-α and expressions of Bax and Bcl-2 in hippocampal neurons in epileptic rats. Anatomy 44(03):204–208

    CAS  Google Scholar 

  • Dmitri P, Tatiana B, Vyacheslav A et al (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37(18):e123

    Google Scholar 

  • Dominguez C, David JM et al (2017) Epithelial-mesenchymal transition and inflammation at the site of the primary tumor. Semin Cancer Biol 47:177–184

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flores EN, García-Aoveros J (2011) TRPML2 and the evolution of mucolipins. Adv Exp Med Biol 704:221–228

    CAS  PubMed  Google Scholar 

  • Fu L, Dong H, Jianhua Y et al (2023) Effects of dietary yeast hydrolysate on the growth performance, intestine health and digestion of juvenile yellow catfish (Pelteobagrus vachelli ♂ × Pelteobagrus fulvidraco ♀). Aquaculture Reports 29:101496

    Google Scholar 

  • Gjin N, Siegmund B et al (2009) Total leucocyte count, but not C-reactive protein, predicts 1-year mortality in patients with acute coronary syndromes treated with percutaneous coronary intervention. Clin Sci 116(8):651–658

    Google Scholar 

  • Gobi N, Vaseeharan B, Chen JC et al (2018) Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 74:8

    Google Scholar 

  • Guo X, Chen DD, Peng KS et al (2016) Identification and characterization of Bacillus subtilis from grass carp (Ctenopharynodon idellus) for use as probiotic additives in aquatic feed. Fish Shellfish Immunol 52:74–84

    CAS  PubMed  Google Scholar 

  • Han B, Long WQ, He JY et al (2015) Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46(2):225–231

    CAS  PubMed  Google Scholar 

  • He L, Chen W, Yang L (2006) Production and partial characterization of bacteriocin-like pepitdes by Bacillus licheniformis ZJU12. Microbiol Res 161(4):321–326

    CAS  PubMed  Google Scholar 

  • Irianto A, Austin B (2010) Use of dead probiotic cells to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 26(1):59–62

    Google Scholar 

  • Kumar R, Mukherjee SC, Ranjan R et al (2008) Enhanced innate immune parameters in Labeo rohita (Ham) following oral administration of Bacillus subtilis. Fish Shellfish Immunol 24(2):168–172

    CAS  PubMed  Google Scholar 

  • Lele Fu, Dong H, Jianhua Yi et al (2023) Effects of dietary yeast hydrolysate on the growth performance, intestine health and digestion of juvenile yellow catfish (Pelteobagrus vachelli ♂ × Pelteobagrus fulvidraco ♀). Aquac Rep 29:101496

    Google Scholar 

  • Li MQ, Zhang ZW (2017) Screening and identification of antagonistic strains of Aeromonas hydrophila, the pathogen of bacterial sepsis in tilapia. Jiangsu Agric Sci 45(3):3

    Google Scholar 

  • Li L, Hu K, Hong B et al (2021a) The inhibitory effect of Bacillus amyloliquefaciens L1 on Aeromonas hydrophila and its mechanism. Aquaculture 539:736590

    CAS  Google Scholar 

  • Li Y, Yang Y, Song L et al (2021b) Effects of dietary supplementation of Lactobacillus plantarum and Bacillus subtilis on growth performance, survival, immune response, antioxidant capacity and digestive enzyme activity in olive flounder (Paralichthys olivaceus). Aquac Fish 6(3):283–288

    Google Scholar 

  • Livermore DM (2004) The need for new antibiotics. Clin Microbiol Infect 10(4):1–9

    PubMed  Google Scholar 

  • Lu Z, Yang M, Zhang K et al (2021) Aeromonas hydrophila infection activates death receptor apoptosis pathway in the red blood cells of grass carp (Ctenopharyngodon idellus). Aquaculture 532:735956

    CAS  Google Scholar 

  • Martirani L, Varcamonti M, Naclerio G et al (2002) Purification and partial characterization of bacillocin 490, a novel bacteriocin produced by a thermophilic strain of Bacillus licheniformis. Microb Cell Fact 1(1):1–1

    PubMed  PubMed Central  Google Scholar 

  • Meidong R, Khotchanalekha K, Doolgindachbaporn S et al (2018) Evaluation of probiotic Bacillus aerius B81e isolated from healthy hybrid catfish on growth, disease resistance and innate immunity of Pla-mong Pangasius bocourti. Fish Shellfish Immunol 73:1–10

    CAS  PubMed  Google Scholar 

  • Mi HF, Sun RJ, Zhang L et al (2015) Research progress of fish gut health. China Feed 15:4

    Google Scholar 

  • Mihaela P, Pertea Geo M, Antonescu Corina M et al (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295

    Google Scholar 

  • Morteza SH, Morteza Y, Alireza A et al (2023) Effects of dietary lactic acid supplementation on the activity of digestive and antioxidant enzymes, gene expressions, and bacterial communities in the intestine of common carp, cyprinus carpio. Animals 13(12):11934

    Google Scholar 

  • Naraghi M, Mehrgan MS, Manouchehri H (2022) Dietary incorporation of Bacillus subtilis and Bacillus licheniformis mixture (DiPro Aqua) ameliorates growth performance, immune response, and intestinal morphology in rainbow trout. N Am J Aquac 84(1):116–125

    Google Scholar 

  • Novo G, Assennato P, Caruso M et al (2009) Clinical significance of macrophage colony stimulating factor levels in acute coronary syndrome. Minerva Cardioangiol 57(1):7–11

    CAS  PubMed  Google Scholar 

  • Ordás MC, Castro R, Dixon B et al (2012) Identification of a novel CCR7 gene in rainbow trout with differential expression in the context of mucosal or systemic infection. Developmental & Comparative Immunology 38(2):302–311

    Google Scholar 

  • Pattnaik P, Kaushik JK, Grover S et al (2010) Purification and characterization of a bacteriocin-like compound (lichenin) produced anaerobically by Bacillus licheniformis isolated from water buffalo. J Appl Microbiol 91(4):636–645

    Google Scholar 

  • Qin L, Yin JG, Zhang W et al (2014) Isolation and identification of pathogenic Aeromonas hydrophila from Esox lucius. Adv Fish Sci 35(05):40–45

    Google Scholar 

  • Rasmussen-Ivey CR, Figueras MJ, Donald MG et al (2016) Virulence factors of Aeromonas hydrophila: in the wake of reclassification. Front Microbiol 7:1337

    PubMed  PubMed Central  Google Scholar 

  • Ren YL, Li Y, Han G et al (2019) Research progress on drug resistance of Aeromonas hydrophila in aquatic products. Chin J Biol Eng 5:7

    Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2020) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140

    Google Scholar 

  • Saftig P, Klumperman J, Saftig P, Klumperman J (2009) Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 10:623–635

    CAS  PubMed  Google Scholar 

  • Settembre C, Fraldi A, Medina DL et al (2013) Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 14:283–296

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen JY (2008) Research progress of Aeromonas hydrophila. J Zhejiang Ocean Univ: Nat Sci Edit 27(1):9

    Google Scholar 

  • Shen WY, Fu LL, Li WF et al (2010) Effect of dietary supplementation with Bacillus subtilis on the growth, performance, immune response and antioxidant activities of the shrimp (Litopenaeus vannamei). Aquac Res 41(11):1691–1698

    CAS  Google Scholar 

  • Song X, Zhao J, Bo Y et al (2014) Aeromonas hydrophila induces intestinal inflammation in grass carp (Ctenopharyngodon idella): an experimental model. Aquaculture 434:171–178

    Google Scholar 

  • Tang XL, Jiang ZY, Cai SY et al (2005) IL-6 down-regulates the expression of tissue factor inhibitor in vascular endothelial cells. J Second Mili Med Univ 26(2):4

    Google Scholar 

  • Wang A, Ran C, Wang Y et al (2008) Use of probiotics in aquaculture of China—a review of the past decade. Fish Shellfish Immunol 86:734–755

    Google Scholar 

  • Wang C R. (2011) Molecular epidemiological investigation of Aeromonas hydrophila and its two typing methods. Ningbo University.

  • Wisel GE, Frazier-Bowers S, D ’Souza RN (2002) Cellular, molecular, and genetic determinants of tooth eruption. Crit Rev Oral Biol Med 13(4):323

    Google Scholar 

  • Wu B, Mottola G, Schaller M et al (2017) Resolution of vascular injury: specialized lipid mediators and their evolving therapeutic implications. Mol Aspects Med 58:72–82

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xing S, Huang C, Mi J et al (2019) Bacillus coagulans R11 maintained intestinal villus health and decreased intestinal injury in lead-exposed mice by regulating the intestinal microbiota and influenced the function of faecal microRNAs. Environ Pollut 255(Pt 2)

  • Yang SM, Wang MS (2006) Aeromonas hydrophila and its pathogenicity to humans. J Dis Cont 5:511–514

    Google Scholar 

  • Yi Y, Zhang Z, Zhao F et al (2018) Probiotic potential of Bacillus velezensis JW: antimicrobial activity against fish pathogenic bacteria and immune enhancement effects on Carassius auratus. Fish Shellfish Immunol 78:322–330

    CAS  PubMed  Google Scholar 

  • Yin Y, Zhang P, Yue X et al (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: bioaccumulation, antioxidant responses and immune responses. Ecotoxicol Environ Saf 161:755–762

    CAS  PubMed  Google Scholar 

  • Yuan XY, Xu RY, Qi Q et al (2022) Dietary fructooligosaccharide and Bacillus licheniformis on growth performance, digestive enzyme, immune indices, and antioxidant capacity of common carp (Cyprinus carpio). Reg Stud Marine Sci 56:102670

    Google Scholar 

  • Zhang DF, Liu LH, Li NQ et al (2015) Epidemiological characteristics of different species of Aeromonas from fish origin in southern my country. Aquat Sci 34(11):10

    CAS  Google Scholar 

  • Zhang CN, Zhang JL, Guan WC et al (2017) Effects of Lactobacillus delbrueckii on immune response, disease resistance against Aeromonas hydrophila, antioxidant capability and growth performance of Cyprinus carpio Huanghe var. Fish Shellfish Immunol 68:84

    CAS  PubMed  Google Scholar 

  • Zhang ML, Shan CJ, Du ZY (2021) Research progress on probiotics and fish gut health. Chin J Fish 1:11

    Google Scholar 

  • Zhao XY, Luo MJ, Li ZG et al (2018) Chromosome-scale assembly of the Monopterus genome. GigaScience 7(5):1–9

    PubMed  Google Scholar 

  • Zhou Y, Zhou QB (2012) Research progress on prevention and control technology of Aeromonas hydrophila. Biohazard Science 2:9

    Google Scholar 

  • Zhou D, Lou Y, Shi W et al (2014) Isolation and Identification of Bacillus Chlamydiae from Aquaculture Land and Screening of Its Amplification Medium 42(7):3

    Google Scholar 

  • Zhu XH, Zhang ZR, Zhou LY et al (2021) Transcriptome analysis of the head kidney of the mandarin fish in the mouth infected by Aeromonas hydrophila. Adv Fish Sci 43:1–11

    Google Scholar 

Download references

Funding

This research was supported by the Jilin Province science and technology development plan key research and development project (20230202076NC) and the Jilin Province modern agricultural industrial technology demonstration and extension project (202301401).

Author information

Authors and Affiliations

Authors

Contributions

Xin-yu Lei: methodology, investigation, validation, formal analysis, writing—original draft. Xin Wang: manuscript revision. Qi-fang Lai: supervision, resources. Peng-cheng Gao: supervision, resources. Xue Cao: supervision, resources. Yue-hong Li: conceptualization, supervision, resources, project administration, formal analysis.

Corresponding author

Correspondence to Yue-hong Li.

Ethics declarations

Ethics approval

The experiment was carried out in accordance with the research plan of the Institutional Animal Care and Use Committee of Jilin Agricultural University.

Consent to participate

All authors agree to participate in this study.

Consent for publication

All authors agree to participate in the publication of this article.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Amany Abbass

Publisher's note

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

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

Lei, Xy., Wang, X., Lai, Qf. et al. Transcriptome analysis of the immunoprotective effect of Bacillus licheniformis on the intestinal tract of Carassius auratus gibelio infected with Aeromonas hydrophila. Aquacult Int 32, 1213–1234 (2024). https://doi.org/10.1007/s10499-023-01213-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-023-01213-5

Keywords

Navigation