Skip to main content

Advertisement

Log in

The effects of amino acids and fatty acids on the disease resistance of Epinephelus fuscoguttatus in response to Vibrio vulnificus infection

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Mass mortality resulting from bacterial infection poses a major problem in the grouper aquaculture industry. The purpose of this study was to profile the metabolites released in challenged fish and to reconstruct the metabolic pathways of brown marble grouper (Epinephelus fuscoguttatus) in response to Vibrio vulnificus infection. Metabolite profiles from control and challenged treatment groups after feeding were determined using gas chromatography–mass spectrometry (GC–MS). Forty metabolites were identified from the GC–MS analysis. These metabolites comprised of amino acids, fatty acids, organic acids and carbohydrates. The profiles showed the highest percent area (33.1%) for leucine from the amino acid class in infected fish compared to the control treatment group (12.3%). Regarding the fatty acid class, a higher percent area of the metabolite 8,11-eicosadienoic acid (27.04%) was observed in fish infected with V. vulnificus than in the control treatment group (22.5%). Meanwhile, in the carbohydrate class, glucose (47.0%) was the metabolite in the carbohydrate class present at highest percentage in the control treatment group compared to infected fish (30.0%). Our findings highlight the importance of a metabolic analysis for understanding the changes of metabolites in E. fuscoguttatus in response to bacterial infections.

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

Similar content being viewed by others

References

  • Abbasi PA, Lazarovits G, Jabaji-Hare S (2009) Detection of high concentrations of organic acids in fish emulsion and their role in pathogen or disease suppression. Phytopathology 99(3):274–281

    CAS  PubMed  Google Scholar 

  • Abumrad NN, Barbul A (2004) The use of arginine in clinical practice. Metabolic and therapeutic aspects of amino acids in clinical nutrition. CRC Press, Boca Raton, Florida, pp 595–611

    Google Scholar 

  • Akayli T, Timur G (2002) Vibriosis in gilthead sea bream (Sparus aurata L.) in farms in the Aegean Sea coast of Turkey. Turk J Fish Aquat Sci 2:89–91

    Google Scholar 

  • Alarcon FJ, Martinez TF, Diaz M, Moyano FJ (2001) Characterization of digestive carbohydrase activity in the gilthead seabream (Sparus aurata). Hydrobiologia 445:199–204

    Google Scholar 

  • Al-Banaw A, Kenngott R, Al-Hassan JM, Mehana N, Sinowatz F (2010) Histochemical analysis of glycoconjugates in the skin of a catfish (Arius tenuispinis, Day). J Vet Med 39(1):42–50

    CAS  Google Scholar 

  • Ampofo JA, Clerk GC (2010) Diversity of bacteria contaminants in tissues of fish cultured in organic waste-fertilized ponds: health implications. Open Fish Sci J 3:142–146

    Google Scholar 

  • Azeredo R, Serra CR, Oliva-Teles A, Costas B (2017) Amino acids as modulators of the European seabass, Dicentrarchus labrax, innate immune response: an in vitro approach. Sci Rep 7:18009

    PubMed  PubMed Central  Google Scholar 

  • Azizan KA, Baharum SN, Noor NM (2012) Metabolic profiling of Lactococcus lactis under different culture conditions. Molecules 17:8022–8036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baharum SN, Nurdalila AA (2011) Phylogenetic Relationships of Epinephelus fuscoguttatus and Epinephelus hexagonatus inferred from mitochondrial cytochrome b gene sequences using bioinformatics tools. Int J Biosci Biochem Bioinf 1(1):47–52

    Google Scholar 

  • Baharum SN, Nurdalila AA (2012) Application of 16s rDNA and cytochrome b ribosomal markers in studies of lineage and fish populations structure of aquatic species. Mol Biol Rep 39(5):5225–5232

    CAS  PubMed  Google Scholar 

  • Brouwer IA, Wanders AJ, Katan MB (2010) Effect of animal and industrial trans fatty acids on HDL and LDL cholesterol levels in humans—a quantitative review. PLoS ONE 5(3):e9434

    PubMed  PubMed Central  Google Scholar 

  • Brown HA, Marnett LJ (2011) Lipid biochemistry, metabolism, and signaling editorial. Chem Rev 111:5817–6512

    CAS  PubMed  Google Scholar 

  • Brugger SD, Baumberger C, Jost M, Jenni W, Brugger U, Mühlemann K (2012) Automated counting of bacterial colony forming units on agar plates. PLoS ONE 7(3):e33695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buentello JA, Gatlin DM (2002) Preliminary observations on the effects of water hardness on free taurine and other amino acids in plasma and muscle of channel catfish. N Am J Aquacult 64:95–102

    Google Scholar 

  • Burnham VE (2006) Strain to strain differences in the growth, survival and adaptation of Vibrio vulnificus and Vibrio parahaemolyticus in broth. Master of Science Thesis, Louisiana State University, USA

  • Charlton M (2006) Branched-chain amino acid enriched supplements as therapy for liver disease. J Nutr 136(1):295S-298S

    CAS  PubMed  Google Scholar 

  • Chatterjee S, Haldar S (2012) Vibrio related diseases in aquaculture and development of rapid and accurate identification methods. J Mar Sci Res Dev 1:002

    Google Scholar 

  • Cronan JE Jr, Subrahmanyam S (1998) FadR, transcriptional co-ordination of metabolic expediency. Mol Microbiol 29:937–943

    CAS  PubMed  Google Scholar 

  • Cronan JE Jr, Waldrop GL (2002) Multi-subunit acetyl-CoA carboxylases. Prog Lipid Res 41:407–435

    CAS  PubMed  Google Scholar 

  • De Bandt JP, Cynober L (2006) Therapeutic use of branchedchain amino acids in burn, trauma, and sepsis. J Nutr 185(1):308S-313S

    Google Scholar 

  • DiRusso CC, Nyström T (1998) The fats of Escherichia coli during infancy and old age: regulation by global regulators, alarm ones and lipid intermediates. Mol Microbiol 27:1–8

    CAS  PubMed  Google Scholar 

  • Etzel MR (2004) Manufacture and use of dairy protein fractions. J Nutr 134(4):996S-1002S

    CAS  PubMed  Google Scholar 

  • Fahy E, Sud M, Cotter D, Subramaniam S (2007) LIPID MAPS online tools for lipid research. Nucleic Acids Res 35:W606-612

    PubMed  PubMed Central  Google Scholar 

  • Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1671–2187

    Google Scholar 

  • Gómez-Requeni P, Mingarro M, Kirchner S, Calduch-Giner JA, Médale F, Corraze G, Panserat S, Martin SAM, Houlihan DF, Kaushik SJ, Pérez-Sánchez J (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture 220(1–4):749–767

    Google Scholar 

  • Guo C, Huang XY, Yang MJ, Wang S, Ren ST, Li H, Peng XX (2014) GC/MS-based metabolomics approach to identify biomarkers differentiating survivals from death in crucian carps infected by Edwardsiella tarda. Fish Shellfish Immunol 39(2):215–222

    CAS  PubMed  Google Scholar 

  • Jia Z, Moulson CL, Pei Z, Miner JH, Watkins PA (2007) Fatty acid transport protein 4 is the principal very long chain fatty acyl-CoA synthetase in skin fibroblasts. J Biol Chem 282:20573–20583

    CAS  PubMed  Google Scholar 

  • Junker BH, Klukas C, Schreiber S (2006) VANTED: a system for advanced data analysis and visualization in the context of biological networks. BMC Bioinf 7:109

    Google Scholar 

  • Kaushik SJ (1998) Whole body amino acid composition of European seabass (Dicentrarchus labrax), gilthead seabream (Sparus aurata) and turbot (Psetta maxima) with an estimation of their IAA requirement profiles. Aquat Living Resour 11(5):355–358

    Google Scholar 

  • Kim JY, Lee JL (2017) Correlation of total bacterial and vibrio spp. populations between fish and water in the aquaculture system. Front Mar Sci 4:1–10

    CAS  Google Scholar 

  • Kim HW, Kim JH, An HS, Park KK, Kim BK, Park T (2003) Myo-inositol restores the inflammation-induced down-regulation of taurine transport by the murine macrophage cell line, RAW 2647. Life Sci 73(19):2477–2489

    CAS  PubMed  Google Scholar 

  • Kim YI, Hirai S, Goto T, Ohyane C, Takahashi H, Tsugane T, Konishi C, Fujii F, Inai S, Iijima Y, Aoki K, Shibata D, Takahashi N, Kawada T (2012) Potent PPARa activator derived from tomato juice, 13-oxo-9, 11-octadecadienoic acid, decreases plasma and hepatic triglyceride in obese diabetic mice. PLoS ONE 7(2):e31317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin CY, Wu H, Tjeerdema RS, Viant MR (2007) Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics 3:55–67

    CAS  Google Scholar 

  • Liu PC, Lin JY, Chuang WH, Lee KK (2004) Isolation and characterization of pathogenic Vibrio harveyi (V. carchariae) from the farmed marine cobia fish Rachycentron canadum L. with gastroenteritis syndrome. World J Microbiol Biotechnol 20:495–499

    Google Scholar 

  • Liu P, Du Y, Meng L, Li X, Liu Y (2016) Metabolic profiling in kidneys of Atlantic salmon infected with Aeromonas salmonicida based on 1 H NMR. Fish Shellfish Immun 58:292–301

    CAS  Google Scholar 

  • Low CF, Mariana NS, Maha A, Chee HY, Fatimah MY (2015) Non-immune-related genes and signaling pathways in spleen of Vibrio parahaemolyticus infected Epinephelus fuscoguttatus (Forskal). J Fish Dis 38:761–764

    CAS  PubMed  Google Scholar 

  • Low CF, Rozaini MZH, Musa N, Baharum SN (2017) Current knowledge of metabolomic approach in infectious fish disease studies. J Fish Dis 40:1267–1277

    PubMed  Google Scholar 

  • Low CF, Shamsir MS, Mohd-Hussien ZA, Baharum SN (2019) Evaluation of potential molecular interaction between quorum sensing receptor, LuxP and grouper fatty acids: In-silico screening and simulation. PeerJ 7:e6568

    PubMed  PubMed Central  Google Scholar 

  • Lu YJ, Rock CO (2006) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566

    CAS  PubMed  Google Scholar 

  • Matsuoka H, Hirooka K, Fujita Y (2007) Organization and function of the YsiA regulon of Bacillus subtilis involved in fatty acid degradation. J Biol Chem 282:5180–5194

    CAS  PubMed  Google Scholar 

  • Mohanty B, Mahanty A, Ganguly S, Sankar TV, Chakraborty K, Rangasamy A, Paul B, Sarma D, Mathew S, Asha KK, Behera B, Aftabuddin M, Debnath D, Vijayagopal P, Sridhar N, Akhtar MS, Sahi N, Mitra T, Banerjee S, Paria P, Das D, Das P, Vijayan KK, Laxmanan PT, Sharma AP (2014) Amino acid compositions of 27 food fishes and their importance in clinical nutrition. J Amino Acids 2014:269797

    PubMed  PubMed Central  Google Scholar 

  • Nik-Haiha NY, Mohd-Zaidi M, Ali HM, Zin RM (2008) The antimicrobial potential of the crude extracts from leaves of some local herbs on fish pathogenic bacteria. http://www.seafdec.org.my/v13/images/stories/pdf/ NaFis2008. Accessed 14 Aug 2019

  • Nurdalila AA, Bunawan H, Kumar SV, Rodrigues KF, Baharum SN (2015) Homogeneous nature of Malaysian marine fish Epinephelus fuscoguttatus (perciformes; serranidae): evidence based on molecular markers, morphology and fourier transform infrared analysis. Int J Mol Sci 16:14884–14900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nurdalila AA, Mayalvanan Y, Baharum SN (2019) Metabolite profiling of Epinephelus fuscoguttatus infected with vibriosis reveal omega 9 as potential metabolite biomarker. Fish Physiol Biochem 45(3):1203–1215

    CAS  PubMed  Google Scholar 

  • Paauw JD, Davis AT (1990) Taurine concentrations in serum of critically injured patients and age- and sex-matched healthy control subjects. Am J Clin Nutr 52:657–660

    CAS  PubMed  Google Scholar 

  • Pan CY, Wang YD, Chen JY (2013) Immunomodulatory effects of dietary Bacillus coagulans in grouper (Epinephelus coioides) and zebrafish (Danio rerio) infected with Vibrio vulnificus. Aquacult Int 21:1155–1168

    Google Scholar 

  • Parry-Billings M, Baigrie RJ, Lamont PM, Morris PJ, Newsholme EA (1992) Effects of major and minor surgery on plasma glutamine and cytokine levels. Arch Surg 127:1237–1240

    CAS  PubMed  Google Scholar 

  • Reed PA, Francis-Floyd R (1996) Vibrio Infections of Fish. University of Florida, Florida, p 31

    Google Scholar 

  • Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio-Rodríguez N, de Diego SM, Beltrán S, Jaime I, Sanz MT, Rovira J (2012) Supercritical fluid extraction of fish oil from fish by-products: a comparison with other extraction methods. J Food Eng 109:238–248

    Google Scholar 

  • Safari D, Marradi M, Chiodo F, Dekker HA, Shan Y, Adamo R, Oscarson S, Rijkers GT, Lahmann M, Kamerling JP, Penadés S, Snippe H (2012) Gold nanoparticles as carriers for a synthetic Streptococcus pneumoniae type 14 conjugate vaccine. Nanomedicine 7(5):651–662

    CAS  PubMed  Google Scholar 

  • Samuelsson LM, Larsson DG (2008) Contributions from metabolomics to fish research. Mol Bio Syst 4(10):974–979

    CAS  Google Scholar 

  • Sarjito S, Radjasa OK, Sabdono A, Prayitno SB, Hutabarat S (2009) Phylogenetic diversity of the causative agents of Vibriosis associated with grouper fish from Karimunjawa Islands, Indonesia. Curr Res Bacteriol 2:14–21

    CAS  Google Scholar 

  • Schujman GE, deMendoza D (2006) Solving an old puzzle in phospholipid biosynthesis. Nat Chem Biol 2:573–574

    CAS  PubMed  Google Scholar 

  • Solanky KS, Burton IW, MacKinnon SL, Walter JA, Dacanay A (2005) Metabolic changes in Atlantic salmon exposed to Aeromonas salmonicida detected by 1H nuclear magnetic resonance spectroscopy of plasma. Dis Aquat Organ 65:107–114

    CAS  PubMed  Google Scholar 

  • Sterzo EV, Paiva JB, Mesquita AL, Freitas NOC, Berchieri A Jr (2007) Organic acids and/or compound with defined microorganisms to control Salmonella enterica serovar Enteritidis experimental infection in chickens. Rev Bras Cienc Avic 9:69–73

    Google Scholar 

  • Thompson FL, Iida T, Swings J (2004) Biodiversity of Vibrios. Microbiol Mol Biol Rev 68:403–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trushina E, Mielke MM (2014) Recent advances in the application of metabolomics to Alzheimer’s disease. Biochem Biophys Acta 1842:1232–1239

    CAS  PubMed  Google Scholar 

  • Uribe C, Folch H, Enriquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med 56(10):486–503

    CAS  Google Scholar 

  • Wu G (2010) Functional amino acids in growth, reproduction, and health. Adv Nutr 1(1):31–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G (2013) Functional amino acids in nutrition and health. Amino Acids 45(3):407–411

    CAS  PubMed  Google Scholar 

  • Yang MJ, Cheng ZX, Jiang M, Zeng ZH, Peng B, Li H (2018) Boosted TCA cycle enhances survival of zebrafish to Vibrio alginolyticus infection. Virulence 9(1):634–644

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young T, Alfaro AC (2016) Metabolomic strategies for aquaculture research: a primer. Rev Aquacult 10(1):26–56

    Google Scholar 

  • Zaman C, Lin K, O’Neill W (2010) The significance and relationships of amino acids and protein in chronic disease and general wellness. Immune Systems Management Inc: 1–15

  • Zhang YM, Marrakchi H, Rock CO (2002) The FabR (YijC) transcription factor regulates unsaturated fatty acid biosynthesis in Escherichia coli. J Biol Chem 77:15558–15565

    Google Scholar 

Download references

Acknowledgements

We also acknowledged Center for Research and Instrumentation Management (CRIM), Universiti Kebangsaan Malaysia (UKM) for the Research Instrumentation Fund (PIP-2010). This work was supported by Research University Grant (GUP-2017-073), Dana Impak Perdana (DIP-2015-024) from Universiti Kebangsaan Malaysia, FRGS/1/2013/SG05/UKM/02/2 from The Ministry of Higher Education, Malaysia (MOHE).

Author information

Authors and Affiliations

Authors

Contributions

SNB conceived and designed the experiments. AAN performed the experiments and analyzed the data. SNB, AAN and MEN wrote and edited the manuscript. All authors reviewed and approved the final version for submission.

Corresponding author

Correspondence to Syarul Nataqain Baharum.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 kb)

Supplementary file2 (DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nurdalila, A.A., Natnan, M.E. & Baharum, S.N. The effects of amino acids and fatty acids on the disease resistance of Epinephelus fuscoguttatus in response to Vibrio vulnificus infection. 3 Biotech 10, 544 (2020). https://doi.org/10.1007/s13205-020-02543-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-02543-4

Keyword

Navigation