Skip to main content
SpringerLink
Log in

Transcriptome analysis of goldfish (Carassius auratus) in response to Gyrodactylus kobayashii infection

  • Immunology and Host-Parasite Interactions - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Gyrodactylid monogeneans are widespread parasites of teleost fishes, and infection with these parasites results in high host morbidity and mortality in aquaculture. To comprehensively elucidate the immune mechanisms against Gyrodactylus kobayashii, the transcriptome profiles of goldfish (Carassius auratus) skin after challenge with G. kobayashii were first investigated using next-generation sequencing. Approximately 21 million clean reads per library were obtained, and the average percentage of these clean reads mapped to the reference genome was 82.25%. A total of 556 differentially expressed genes (DEGs), including 344 upregulated and 212 downregulated genes, were identified, and 380 DEGs were successfully annotated and assigned to 95 signaling pathways in Kyoto Encyclopedia of Genes and Genomes (KEGG). In addition, 14 pathways associated with immune response were identified mainly including mTOR signaling pathway, cytokine-cytokine receptor interaction, intestinal immune network for IgA production, toll-like receptor signaling pathway, and phagosome. Twelve genes were selected and validated using qRT-PCR. A similar trend of these genes between RNA-Seq and qRT-PCR was observed, indicating that RNA-Seq data was reliable. Besides, the ALP activity and NO content in serum were significantly higher in the infected goldfish compared with the non-infected goldfish. In summary, this study provides better understandings of immune defense mechanisms of goldfish against G. kobayashii, which will support future molecular research on gyrodactylids and facilitate the prevention and treatment of gyrodactylosis in aquaculture.

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

Similar content being viewed by others

References

  • Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Adv Parasitol 64:161–376

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57(1):289–300

    Google Scholar 

  • Bogdan C, Mattner J, Schleicher U (2004) The role of type I interferons in non-viral infections. Immunol Rev 202:33–48

    Article  CAS  Google Scholar 

  • Boneberg E-M, Hartung T (2002) Molecular aspects of anti-inflammatory action of G-CSF. Inflamm Res 51(3):119–128

    Article  CAS  Google Scholar 

  • Brunet LR (2001) Nitric oxide in parasitic infections. Int Immunopharmacol 1(8):1457–1467

    Article  CAS  Google Scholar 

  • Buchmann K (1999) Immune mechanisms in fish skin against monogeneans-a model. Folia Parasitol 46(1):1–8

    CAS  Google Scholar 

  • Cable J, Harris PD (2002) Gyrodactylid developmental biology: historical review, current status and future trends. Int J Parasitol 32(3):255–280

    Article  CAS  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890

    Article  Google Scholar 

  • Collins CM et al (2007) Isolation of a FIP2-like gene from Atlantic salmon (Salmo salar L.), found upregulated following infection with the monogenean parasite Gyrodactylus salaris Malmberg, 1957. Fish Shellfish Immunol 22(3):282–288

    Article  CAS  Google Scholar 

  • Comerford I, Milasta S, Morrow V, Milligan G, Nibbs R (2006) The chemokine receptor CCX-CKR mediates effective scavenging of CCL19 in vitro. Eur J Immunol 36(7):1904–1916

    Article  CAS  Google Scholar 

  • Hu YZ, Li AX, Xu Y, Jiang B, Lu GL, Luo XC (2017) Transcriptomic variation of locally-infected skin of Epinephelus coioides reveals the mucosal immune mechanism against Cryptocaryon irritans. Fish Shellfish Immunol 66:398–410

    Article  CAS  Google Scholar 

  • IBM Corp (2011) IBM SPSS Statistics for Windows, Version 20.0. IBM Corp, New York

    Google Scholar 

  • Jorgensen TR, Raida MK, Kania PW, Buchmann K (2009) Response of rainbow trout (Oncorhynchus mykiss) in skin and fin tissue during infection with a variant of Gyrodactylus salaris (Monogenea: Gyrodactylidae). Folia Parasitol 56(4):251–258

    Article  Google Scholar 

  • Keating R, McGargill MA (2016) mTOR regulation of lymphoid cells in immunity to pathogens. Front Immunol 7:180

  • Keita M, Vincendeau P, Buguet A, Cespuglio R, Vallat JM, Dumas M, Bouteille B (2000) Inducible nitric oxide synthase and nitrotyrosine in the central nervous system of mice chronically infected with Trypanosoma brucei brucei. Exp Parasitol 95(1):19–27

    Article  CAS  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36

    Article  Google Scholar 

  • Lallès J-P (2019) Biology, environmental and nutritional modulation of skin mucus alkaline phosphatase in fish: a review. Fish Shellfish Immun 89:179–186

    Article  Google Scholar 

  • Lalles J-P (2014) Intestinal alkaline phosphatase: novel functions and protective effects. Nutr Rev 72(2):82–94

    Article  Google Scholar 

  • Li Y, Xu W, Li X, Jiang H, She Q, Han Z, Li X, Chen Q (2018) Comparative transcriptome analysis of Chinese grass shrimp (Palaemonetes sinensis) infected with isopod parasite Tachaea chinensis. Fish Shellfish Immunol 82:153–161

    Article  CAS  Google Scholar 

  • Lin Y-C, Chen JC, Chen YY, Liu CH, Cheng W, Hsu CH, Tsui WC (2013) Characterization of white shrimp Litopenaeus vannamei integrin β and its role in immunomodulation by dsRNA-mediated gene silencing. Dev Comp Immunol 40(2):167–179

    Article  CAS  Google Scholar 

  • Matejusova I et al (2006) Gene expression profiles of some immune relevant genes from skin of susceptible and responding Atlantic salmon (Salmo salar L.) infected with Gyrodactylus safaris (Monogenea) revealed by suppressive subtractive hybridisation. Int J Parasitol 36(10–11):1175–1183

    Article  CAS  Google Scholar 

  • Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33(10):789–801

    Article  CAS  Google Scholar 

  • Schelkle B, Shinn AP, Peeler E, Cable J (2009) Treatment of gyrodactylid infections in fish. Dis Aquat Org 86(1):65–75

    Article  Google Scholar 

  • Sedger LM, Seddiki N, Ranasinghe C (2014) Cytokines and cytokine receptors as immunotherapeutics: humble beginnings and exciting futures. Cytokine Growth Factor Rev 25(4):351–353

    Article  CAS  Google Scholar 

  • Shapira M, Zinoviev A (2011) Leishmania parasites act as a trojan horse that paralyzes the translation system of host macrophages. Cell Host Microbe 9(4):257–259

    Article  CAS  Google Scholar 

  • Silke J, Brink R (2009) Regulation of TNFRSF and innate immune signalling complexes by TRAFs and cIAPs. Cell Death Differ 17:35

    Article  Google Scholar 

  • Silva-Santos B (2012) Driving IL-17+ γδ T-cell migration in allergic reactions: a new “inflammatory” role for the “homeostatic” chemokine CCL25. Eur J Immunol 42(5):1097–1101

    Article  CAS  Google Scholar 

  • Sterud, Harris, Bakke (1998) The influence of Gyrodactylus salaris Malmberg 1957 (Monogenea) on the epidermis of Atlantic salmon, Salmo salar L., and brook trout, Salvelinus fontinalis (Mitchill): experimental studies. J Fish Dis 21(4):257–263

    Article  CAS  Google Scholar 

  • Sudhagar A, Ertl R, Kumar G, El-Matbouli M (2019) Transcriptome profiling of posterior kidney of brown trout, Salmo trutta, during proliferative kidney disease. Parasit Vectors 12(1):569

    Article  CAS  Google Scholar 

  • Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2012) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31:46

    Article  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  Google Scholar 

  • Tu X, Qi X, Huang A, Ling F, Wang G (2019) Cytokine gene expression profiles in goldfish (Carassius auratus) during Gyrodactylus kobayashii infection. Fish Shellfish Immunol 86:116–124

    Article  CAS  Google Scholar 

  • Wang P, Wang J, Su YQ, Mao Y, Zhang JS, Wu CW, Ke QZ, Han KH, Zheng WQ, Xu ND (2016) Transcriptome analysis of the Larimichthys crocea liver in response to Cryptocaryon irritans. Fish Shellfish Immunol 48:1–11

    Article  Google Scholar 

  • Wen J, Song C, Liu J, Chen J, Zhai X, Hu Z (2016) Expression quantitative trait loci for TNFRSF10 influence both HBV infection and hepatocellular carcinoma development. J Med Virol 88(3):474–480

    Article  CAS  Google Scholar 

  • Yin F, Gao Q, Tang B, Sun P, Han K, Huang W (2016) Transcriptome and analysis on the complement and coagulation cascades pathway of large yellow croaker (Larimichthys crocea) to ciliate ectoparasite Cryptocaryon irritans infection. Fish Shellfish Immunol 50:127–141

    Article  CAS  Google Scholar 

  • Zhou S, Li WX, Wang YQ, Zou H, Wu SG, Wang GT (2017a) Anthelmintic efficacies of three common disinfectants and extracts of four traditional Chinese medicinal plants against Gyrodactylus kobayashii (Monogenea) in goldfish (Carassius auratus). Aquaculture 466:72–77

    Article  CAS  Google Scholar 

  • Zhou S, Li WX, Zou H, Zhang J, Wu SG, Li M, Wang GT (2018) Expression analysis of immune genes in goldfish (Carassius auratus) infected with the monogenean parasite Gyrodactylus kobayashii. Fish Shellfish Immunol 77:40–45

    Article  CAS  Google Scholar 

  • Zhou S, Zou H, Wu SG, Wang GT, Marcogliese DJ, Li WX (2017b) Effects of goldfish (Carassius auratus) population size and body condition on the transmission of Gyrodactylus kobayashii (Monogenea). Parasitology 144(9):1221–1228

    Article  CAS  Google Scholar 

  • Zou J, Redmond AK, Qi Z, Dooley H, Secombes CJ (2015) The CXC chemokine receptors of fish: insights into CXCR evolution in the vertebrates. Gen Comp Endocrinol 215:117–131

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by China Postdoctoral Science Foundation (2018M642964), Postdoctoral Innovation Project of Hubei Province (2019), National Natural Science Foundation of China (31902417), and Central Public-interest Scientific Institution Basal Research Fund (2019ZD0901).

Author information

Authors and Affiliations

  1. Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, No. 8 Wuda Park Road 1, Wuhan, 430223, Hubei Province, China

    Shun Zhou, Yongtao Liu, Jing Dong, Qiuhong Yang, Ning Xu, Yibin Yang & Xiaohui Ai

  2. Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, 430223, China

    Shun Zhou & Zemao Gu

  3. Hu Bei Province Engineering and Technology Research Center of Aquatic Product Quality and Safety, Wuhan, 430223, China

    Shun Zhou, Yongtao Liu, Jing Dong, Qiuhong Yang, Ning Xu, Yibin Yang & Xiaohui Ai

Authors
  1. Shun Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongtao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiuhong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ning Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yibin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zemao Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaohui Ai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaohui Ai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: Shokoofeh Shamsi

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 273 kb)

ESM 2

(XLSX 208 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, S., Liu, Y., Dong, J. et al. Transcriptome analysis of goldfish (Carassius auratus) in response to Gyrodactylus kobayashii infection. Parasitol Res 120, 161–171 (2021). https://doi.org/10.1007/s00436-020-06827-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06827-9

Keywords

Search

Navigation