Molecular Biology Reports

, Volume 45, Issue 6, pp 2511–2523 | Cite as

A comparative transcriptome approach for identification of molecular changes in Aphanomyces invadans infected Channa striatus

  • Venkatesh Kumaresan
  • Mukesh Pasupuleti
  • Mariadhas Valan Arasu
  • Naif Abdullah Al-Dhabi
  • Aziz Arshad
  • S. M. Nurul Amin
  • Fatimah Md. Yusoff
  • Jesu ArockiarajEmail author
Original Article


Snakehead murrel, Channa striatus is an economically important aquatic species in Asia and are widely cultured and captured because of its nutritious and medicinal values. Their growth is predominantly affected by epizootic ulcerative syndrome (EUS) which is primarily caused by an oomycete fungus, Aphanomyces invadans. However, the molecular mechanism of immune response in murrel against this infection is still not clear. In this study, transcriptome technique was used to understand the molecular changes involved in C. striatus during A. invadans infection. RNA from the control (CF) and infected fish (IF) groups were sequenced using Illumina Hi-seq sequencing technology. For control group, 28,952,608 clean reads were generated and de novo assembly was performed to produce 60,753 contigs. For fungus infected group, 25,470,920 clean reads were obtained and assembled to produce 58,654 contigs. Differential gene expression analysis revealed that a total of 146 genes were up-regulated and 486 genes were down regulated. Most of the differentially expressed genes were involved in innate immune mechanism such as pathogen recognition, signalling and antimicrobial mechanisms. Interestingly, few adaptive immune genes, especially immunoglobulins were also significantly up regulated during fungal infection. Also, the results were validated by qRT-PCR analysis. These results indicated the involvement of various immune genes involved in both innate and adaptive immune mechanism during fungal infection in C. striatus which provide new insights into murrel immune mechanisms against A. invadans.


Snakehead Murrel Aphanomyces invadans Epizootic ulcerative syndrome Transcriptome Gene expression 



Epizootic ulcerative syndrome


Control fish


Infected fish


World Organisation for Animal Health


Mycotic granulomatosis


Red spot disease


Ulcerative mycosis


Next generation sequencing


Fragments per kilobase of exon per million fragments mapped


Gene ontology


Molecular function


Cellular component


Biological process


Quantitative real-time polymerase chain reaction


Quantification cycle


Pattern recognition receptors


Pathogen-associated molecular patterns


Peptidoglycan recognition proteins




Nonspecific cytotoxic cells


Natural killer

PGC 1α

Peroxisome proliferator-activated receptor gamma co-activator 1 alpha


Oxidative phosphorylation


Carnitine palmitoyl transferase I




Leukocyte immune-type receptor


Immunoglobulin superfamily


Alternate pathway



This research is supported by Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India, New Delhi under the program of Aquaculture and Marine Biotechnology (No. BT/PR13183/AAQ/3/723/2015). The authors also grateful to the Deanship of Scientific Research, King Saud University for partial funding through Vice Deanship of Scientific Research Chairs. Moreover, the corresponding author would like to acknowledge Institute of Bioscience, Universiti Putra Malaysia, Malaysia for providing him visiting professor Award (UPM/PEND/500-3/4/10) to complete this study under the HICoE and SATREPS-COSMOS programs, Ministry of Higher Education Malaysia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human and animal participants

This experiment does not contain any human participants. The animal, striped murrel Channa striatus used in this experiment was treated with care following the ethical procedures of the SRM Institute of Science and Technology (SRMIST) guidelines and regulations. All the experimental protocols were approved by the research committee of SRMIST.

Supplementary material

11033_2018_4418_MOESM1_ESM.docx (285 kb)
Supplementary material 1 (DOCX 284 KB)


  1. 1.
    Arockiaraj J, Sathyamoorthi A, Kumaresan V, Palanisamy R, Chaurasia MK, Bhatt P, Gnanam AJ, Pasupuleti M, Arasu A (2014) A murrel interferon regulatory factor-1: molecular characterization, gene expression and cell protection activity. Mol Biol Rep 41:5299–5309CrossRefGoogle Scholar
  2. 2.
    Robledo D, Taggart JB, Ireland JH (2016) Gene expression comparison of resistant and susceptible Atlantic salmon fry challenged with infectious pancreatic necrosis virus reveals a marked contrast in immune response. BMC Genom 17:279CrossRefGoogle Scholar
  3. 3.
    Lilley J, Callinan R, Chinabut S, Kanchanakhan S, MacRae I (1998) Epizootic ulcerative syndrome (EUS) technical handbook. The Aquatic Animal Health Institute, BankokGoogle Scholar
  4. 4.
    OIE (2013) Chap. 2.3.2. Infection with Aphanomyces invadans (Epizootic ulcerative syndrome). In: Hnin Thidar Myint (ed) Manual of diagnostic tests for aquatic animals. Oie World Organisation for Animal Health, ParisGoogle Scholar
  5. 5.
    Dhanaraj M, Haniffa MA, Ramakrishnan CM, Arunsingh SV (2008) Microbial flora from the epizootic ulcerative syndrome (EUS) infected murrel Channa striatus (Bloch, 1797) in Tirunelveli region. Turk J Vet Anim Sci 32:221–224Google Scholar
  6. 6.
    John KR, George MR (2012) Viruses associated with epizootic ulcerative syndrome: an update. Indian J Virol 23:106–113CrossRefGoogle Scholar
  7. 7.
    Ahmed M, Rab MA (1995) Factors affecting outbreaks of epizootic ulcerative syndrome in farmed and wild fish in Bangladesh. J Fish Dis 18:263–271CrossRefGoogle Scholar
  8. 8.
    Andrew TG, Huchzermeyer KDA, Mbeha BC, Nengu SM (2008) Epizootic ulcerative syndrome affecting fish in the Zambezi river system in southern Africa. Vet Rec 163:629–631CrossRefGoogle Scholar
  9. 9.
    Boys CA, Rowland SJ, Gabor M, Gabor L, Marsh IB (2012) Emergence of epizootic ulcerative syndrome in native fish of the Murray-Darling river system, Australia: hosts, distribution and possible vectors. PLoS ONE 7(4):e35568CrossRefGoogle Scholar
  10. 10.
    Kong F, You H, Tang R, Zheng K (2017) The regulation of proteins associated with the cytoskeleton by hepatitis B virus X protein during hepatocarcinogenesis. Oncol Lett 13(4):2514–2520CrossRefGoogle Scholar
  11. 11.
    Lüder CGK, Lang T, Beuerle B, Gross U (1998) Down-regulation of MHC class II molecules and inability to up-regulate class I molecules in murine macrophages after infection with Toxoplasma gondii. Clin Exp Immunol 112(2):308–316CrossRefGoogle Scholar
  12. 12.
    Li X, Wang S, Qi J, Echtenkamp SF, Chatterjee R, Wang M, Boons GJ, Dziarski R, Gupta D (2007) Zebrafish peptidoglycan recognition proteins are bactericidal amidases essential for defense against bacterial infections. Immunity 27(3):518–529CrossRefGoogle Scholar
  13. 13.
    Jaso-Friedmann L, Leary JH, Evans DL (1997) NCCRP-1: a novel receptor protein sequenced from teleost nonspecific cytotoxic cells. Mol Immunol 34(12–13):955–965CrossRefGoogle Scholar
  14. 14.
    Bajoghli B (2013) Evolution and function of chemokine receptors in the immune system of lower vertebrates. Eur J Immunol 43(7):1686–1692CrossRefGoogle Scholar
  15. 15.
    Arockiaraj J, Bhatt P, Kumaresan V, Dhayanithi NB, Arshad A, Harikrishnan R, Arasu MV, Al-Dhabi NA (2015) Fish chemokines 14, 20 and 25: a comparative statement on computational analysis and mRNA regulation upon pathogenic infection. Fish Shellfish Immunol 47(1):221–230CrossRefGoogle Scholar
  16. 16.
    Palanisamy R, Bhatt P, Kumaresan V, Pasupuleti M, Arockiaraj J (2016) Innate and adaptive immune molecules of striped murrel Channa striatus. Rev Aquac. CrossRefGoogle Scholar
  17. 17.
    Wan X, Wen JJ, Koo SJ, Liang LY, Garg NJ (2016) SIRT1-PGC1α-NFκB pathway of oxidative and inflammatory stress during Trypanosoma cruzi infection: benefits of SIRT1-targeted therapy in improving heart function in chagas disease. PLoS Pathog 12(10):e1005954CrossRefGoogle Scholar
  18. 18.
    Luhachack LG, Visvikis O, Wollenberg AC, Lacy-Hulbert A, Stuart LM, Irazoqui JE (2012) EGL-9 controls C. elegans host defense specificity through prolyl hydroxylation-dependent and -independent HIF-1 pathways. PLoS Pathogen 8(7):e1002798CrossRefGoogle Scholar
  19. 19.
    Bhandari T, Nizet V (2014) Hypoxia-inducible factor (HIF) as a pharmacological target for prevention and treatment of infectious diseases. Infect Dis Ther 3(2):159–174CrossRefGoogle Scholar
  20. 20.
    Morash AJ, Kajimura M, McClelland GB (2008) Inter tissue regulation of carnitine palmitoyl transferase I (CPTI): mitochondrial membrane properties and gene expression in rainbow trout (Oncorhynchus mykiss). Biochim Biophys Acta 1778:1382–1389CrossRefGoogle Scholar
  21. 21.
    Brothers KM, Newman ZR, Wheeler RT (2011) Live imaging of disseminated candidiasis in zebrafish reveals role of phagocyte oxidase in limiting filamentous growth. Eukaryot Cell 10(7):932–944CrossRefGoogle Scholar
  22. 22.
    Braceland M, Bickerdike R, Tinsley J, Cockerill D, Mcloughlin MF, Graham DA, Eckersall PD (2013) The serum proteome of Atlantic salmon, Salmo salar, during pancreas disease (PD) following infection with salmonid alphavirus subtype 3 (SAV3). J Proteom 94:423–436CrossRefGoogle Scholar
  23. 23.
    Porcellini A, Iacovelli L, De Blasi A (2011) Viral infection for GPCR expression in eukaryotic cells. Methods Mol Biol 746:39–51CrossRefGoogle Scholar
  24. 24.
    Stratos I, Rotter R, Eipel C, Mittlmeier T, Vollmar B (2007) Granulocyte-colony stimulating factor enhances muscle proliferation and strength following skeletal muscle injury in rats. J Appl Physiol 103(5):1857–1863CrossRefGoogle Scholar
  25. 25.
    Zelante T, Wong AYW, Mencarelli A, Foo S, Zolezzi F, Lee B, Poidinger M, Ricciardi-Castagnoli P, Fric J (2017) Impaired calcineurin signalling in myeloid cells results in down regulation of pentraxin-3 and increased susceptibility to aspergillosis. Mucosal Immunol 10:470–480CrossRefGoogle Scholar
  26. 26.
    Arasu A, Kumaresan V, Palanisamy R, Arasu MV, Al-Dhabi NA, Ganesh MR, Arockiaraj J (2017) Bacterial membrane binding and pore formation abilities of carbohydrate recognition domain of fish lectin. Dev Comp Immunol 67:202–212CrossRefGoogle Scholar
  27. 27.
    Kumaresan V, Bhatt P, Ganesh MR, Harikrishnan R, Arasu M, Al-Dhabi NA, Pasupuleti M, Marimuthu K, Arockiaraj J (2015) A novel antimicrobial peptide derived from fish goose type lysozyme disrupts the membrane of Salmonella enterica. Mol Immunol 68(2 Pt B):421–433CrossRefGoogle Scholar
  28. 28.
    Hardison SE, Brown GD (2012) C-type lectin receptors orchestrate anti-fungal immunity. Nat Immunol 13(9):817–822CrossRefGoogle Scholar
  29. 29.
    Samaranayake YH, Cheung BP, Parahitiyawa N, Seneviratne CJ, Yau JY, Yeung KW, Samaranayake LP (2009) Synergistic activity of lysozyme and antifungal agents against Candida albicans biofilms on denture acrylic surfaces. Arch Oral Biol 54(2):115–126CrossRefGoogle Scholar
  30. 30.
    Magalhães GS, Lopes-Ferreira M, Junqueira-de-Azevedo IL, Spencer PJ, Araújo MS, Portaro FC, Ma L, Valente RH, Juliano L, Fox JW, Ho PL, Moura-da-Silva AM (2005) Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie 87(8):687–699CrossRefGoogle Scholar
  31. 31.
    Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:459CrossRefGoogle Scholar
  32. 32.
    Sunyer JO (2013) Fishing for mammalian paradigms in the teleost immune system. Nat Immunol 14(4):320–326CrossRefGoogle Scholar
  33. 33.
    Takada A, Watanabe S, Ito H, Okazaki K, Kida H, Kawaoka Y (2000) Down regulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology 278(1):20–26CrossRefGoogle Scholar
  34. 34.
    Onodera T, Poe JC, Tedder TF, Tsubata T (2008) CD22 regulates time course of both B cell division and antibody response. J Immunol 180(2):907–913CrossRefGoogle Scholar
  35. 35.
    Nguyen T, Liu XK, Zhang Y, Dong C (2006) BTNL2, a butyrophilin-like molecule that functions to inhibit T cell activation. J Immunol 176(12):7354–7360CrossRefGoogle Scholar
  36. 36.
    Draborg AH, Lydolph MC, Westergaard M, Olesen Larsen S, Nielsen CT, Duus K, Jacobsen S, Houen G (2015) Elevated concentrations of serum immunoglobulin free light chains in systemic lupus erythematosus patients in relation to disease activity, inflammatory status, B cell activity and Epstein-Barr virus antibodies. PLoS One 10(9):e0138753CrossRefGoogle Scholar
  37. 37.
    Dunkelberger JR, Song WC (2010) Complement and its role in innate and adaptive immune responses. Cell Res 20(1):34–50CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biotechnology, Faculty of Science and HumanitiesSRM Institute of Science and TechnologyChennaiIndia
  2. 2.Lab PCN 206, Microbiology DivisionCSIR-Central Drug Research InstituteLucknowIndia
  3. 3.Addiriyah Research Chair for Environmental Studies, Department of Botany and Microbiology, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  4. 4.International Institute of Aquaculture and Aquatic Sciences (I-AQUAS), Universiti Putra MalaysiaSi Rusa Port DicksonMalaysia
  5. 5.Department of Aquaculture, Faculty of AgricultureUniversiti Putra MalaysiaSerdangMalaysia
  6. 6.Laboratory of Marine Biotechnology, Institute of BioscienceUniversiti Putra MalaysiaSerdangMalaysia
  7. 7.SRM Research InstituteSRM Institute of Science and TechnologyChennaiIndia

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