Log in

Alternations in the liver metabolome, skin and serum antioxidant function of silver pomfret (Pampus Argenteus) is induced by jellyfish feeding

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

Abstract

Many fish species are known to feed on jellyfish. Herein, we observed the effects of jellyfish feeding on silver pomfret using gas chromatography tandem time-of-flight mass spectrometry (GC-TOF–MS) based on metabolomics. We studied the effects of feeding on jellyfish on skin and serum immune of silver pomfret. Healthy silver pomfret (initial weight, 13.40 ± 1.565 g) was divided into two groups: control and feeding. The pomfrets were fed jellyfish at 2, 6, 12, 24, and 72 h, and samples were obtained. Statistical analysis revealed that after jellyfish feeding, most serum immune indicators did not show a significant change; however, skin immune indicators indicated that silver pomfret elicit a stress response on encountering jellyfish, gradually adapting to their presence. We therefore conducted further experiments involving two groups: group A, which was not fed any extra jellyfish, and group B, which was fed extra jellyfish (approximately 10% weight of silver pomfret) every day for 60 days. Orthogonal partial least squares discriminant analysis led to the identification of stronger biomarkers, with the liver metabolome showing obvious variations between the groups (group B vs. A). After feeding jellyfish by silver pomfret, some amino acids, amines, and unsaturated fatty acids in the liver tissue showed a significant increase. Our results, thus, not only reveal changes in physiological indices of silver pomfret after feeding on jellyfish but also provide a new idea for further optimizing the feed formula for silver pomfret culture.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17

Similar content being viewed by others

References

  • Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85:523–536

    Article  Google Scholar 

  • Arai MN, Welch DW, Dunsmuir AL, Jacobs MC, Ladoucer AR (2003) Digestion of pelagic Ctenophora and Cnidaria by fish. Can J Fish Aquat Sci 60:825–829

    Article  Google Scholar 

  • Assis CRDD, Linhares AG, Oliveira VM, França RCP, Santos JF, Marcuschi M, Carvalho EVVV, BezerraJunior RSLBC (2014) Characterization of catalytic efficiency parameters of brain cholinesterases in tropical fish. Fish Physiol Biochem 40(6):1659–1668

    Article  Google Scholar 

  • Becker AG, Parodi TV, Gonçalves JF, Bagatini MD, Spanevello RM, Morsch VM, Schetinger MRC, Baldisserotto B (2013) Ectonucleotidase and acetylcholinesterase activities in silver catfish (Rhamdia quelen) exposed to different salinities. Biochem Syst Ecol 46:44–49

    Article  CAS  Google Scholar 

  • Calabrese EJ (2005) Paradigm lost, paradigm found: The reemergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138(3):378–411

    Article  CAS  Google Scholar 

  • Cai XX, Su XR, Yang C, Li H (2008) Activity detection and extraction of jellyfish venom. Fisheries Sci 3:145–147

    Google Scholar 

  • Cardona L, Álvarez de Quevedo I, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE 7(3):e31329

    Article  CAS  Google Scholar 

  • Chen Q, Luo SL, Zhang-Sun DT (2007) Research development of jellyfish toxins. Biotechnology 17(6):95–97

    CAS  Google Scholar 

  • Covello JM, Bird S, Morrison RN, Bridle AR, Battaglene SC, Secombes CJ, Nowak BF (2013) Isolation of RAG-1 and IgM transcripts from the striped trumpeter (Latris lineata), and their expression as markers for development of the adaptive immune response. Fish Shellfish Immunol 34(3):778

    Article  CAS  Google Scholar 

  • Doyle TK, Houghton JDR, McDevitt R, Davenport J, Hays GC (2007) The energy density of jellyfish: estimates frombomb-calorimetry and proximate-composition. J Exp Mar Bio Ecol 343(2):239–252

    Article  Google Scholar 

  • Esteban MA (2012) An overview of the immunological defenses in fish skin. Isrn immunology 2012:3–4

    Google Scholar 

  • Fan CP, Wang Q, Liu XY, Li GY, Li KB (2011) Toxicity and effect of tetrabromodiphenyl ether upon the antioxidant defense system of swordtail fish (**phophorus helleri). Acta Sci Circum 31(3):642–648

    CAS  Google Scholar 

  • Garcia A, Barbas C (2011) Gas chromatography-mass spectrometry (GC-MS)-based metabolomics. Methods Mol Biol 708:191–204

    Article  CAS  Google Scholar 

  • Gong H, Wu SQ, Pan H (2006) Summary on Mucosal Immunity System and Mechanism in Teleost. Progress In Veterinary Medicine 27(6):24–28

    Google Scholar 

  • Han CY, Zheng QM, Chen GD, Liu LX (2014) Effect of ammonia-N stress on non-specific immunity of tilapia (Oreochromis niloticus × O. areus). South China Fisheries Science 10(3):47–52

    Google Scholar 

  • Huang ZH, Ma AJ, Lei JL (2013) Progress in study on the skin mucus lectin in fish. Dongwuxue Yanjiu 34(6):674–679

    PubMed  Google Scholar 

  • Jennifer EP, Mary NA (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451:27–44

    Article  Google Scholar 

  • Jiang H, Cheng HQ, Xu HG, Arreguín-Sánchez F, Quesne WL (2010) Impact of large jellyfish bloom on energy balance of middle and upper ecosystem in East China Sea. Mar Environ Res 29(1):91–95

    Google Scholar 

  • Kanak EG, Dogan Z, Eroglu A, Atli G, Canli M (2014) Effects of fish size on the response of antioxidant systems of Oreochromis niloticus following metal exposures. Fish Physiol Biochem 40(4):1083–1091

    CAS  PubMed  Google Scholar 

  • Li SF, Cheng JH, Li CS, Li JS (2005) Seasonal Changes on fish community diversity in the middle part of the East China Sea. Marine Fisheries 27(2):113–119

    Google Scholar 

  • Liu CS, Zhuang ZM, Chen SQ, Shi ZH, Yan JP, Liu CL (2014) Medusa consumption and prey selection of silver pomfret Pampus argenteus juveniles. Chin J Oceanol Limn 32:71–80

    Article  Google Scholar 

  • Milisenda G, Rosa S, Fuentes VL, Boero F, Guglielmo L, Purcell JE, Piraino S (2014) Jellyfish as prey: frequency of predation and selective foraging of boops boops (Vertebrata, Actinopterygii) on the mauve stinger pelagia noctiluca (Cnidaria, Scyphozoa). PLoS ONE 9(4):e94600

    Article  Google Scholar 

  • Miyajima-Taga Y, Masuda R, Morimitsu R, Ishii H, Nakajima K, Hydrobiologia YY (2016) Ontogenetic changes in the predator–prey interactions between threadsail filefish and moon jellyfish. Hydrobiologia 772(1):175–187

    Article  CAS  Google Scholar 

  • Parker S, La FA, Salinas I (2012) The ontogeny of New Zealand groper (Polyprion oxygeneios) lymphoid organs and IgM. Dec Comp Immunol 38(2):215

    Article  CAS  Google Scholar 

  • Pati S (1980) Food and feeding habits of silver pomfret Pampus argenteus(Euphrasen) from Bay of Bengal with a note on its significance in fishery. Indian J Fish 27:244–256

    Google Scholar 

  • Peng SM, Shi ZH, Yin F, Sun P, Wang JG (2011) Feeding habits of silver pomfret (Pampus argenteus) in East China Sea based on stable isotope techniques. Chinese J Ecol 30(7):1565–1569

    Google Scholar 

  • Pilström L, Bengtén E (1996) Immunoglobulin in fish-genes, expression and structure. Fish Shellfish Immunol 6(4):243–262

    Article  Google Scholar 

  • Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 4:209–235

    Article  Google Scholar 

  • Swain P, Nayak SK (2009) Role of maternally derived immunity in fish. Fish Shellfish Immunol 27(2):89–99

    Article  CAS  Google Scholar 

  • Shi ZH, Zhang YL, Gao QX, Peng SM, Zhang CJ (2015) Dietary vitamin E level affects the response of juvenile epinehelus moara to ammonia nitrogen stress. Chin J Anim Nutr 5:1596–1604

    Google Scholar 

  • Trygg J, Wold S (2002) Orthogonal projections to latent structures (O-PLS). J Chemom 16(3):119–128

    Article  CAS  Google Scholar 

  • Tsugawa H, Tsujimoto Y, Arita M et al (2011) GC/MS based metabolomics: development of a data mining system for metabolite identification by using soft independent modeling of class analogy (SIMCA). BMC Bioinform 12(1):1

    Article  Google Scholar 

  • Wang HB, Lu J, Kuikarni S, Zhang WQ, Gorka JE, Mandel JA, Goetzman ES, Prochownik EV (2019) Metabolic and oncogenic adaptations to pyruvate dehydrogenase inactivation in fibroblasts. J Biol Chem 294:5466–5486

    Article  CAS  Google Scholar 

  • Wang JY, Bian HF, ** XQ, Sheng LX (2009) Stress and biological response of naphthalene on the antioxidant defense system in visceral mass of zebrafish. Environ Sci 30(2):516–521

    CAS  Google Scholar 

  • Wang ZP, Zhang SC, Wang GF (2008) Advances on the complement components, characteristic and function of complement system in fish. Acta Hydrobiol Sin 32(5):760–769

    Article  CAS  Google Scholar 

  • Wiklund S, Johansson E, Sjoestroem L, Mellerowicz EJ, Edlund U, Shockcor JP, Gottfries J, Moritz T, Trygg J (2008) Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. Anal Chem 80(1):115–122

    Article  CAS  Google Scholar 

  • **ao L, Zhang LM (2007) Research development of jellyfish toxins. Chin J Mar Drugs 26(6):40–43

    CAS  Google Scholar 

  • Zhang S, Wang Z, Wang H (2013) Maternal immunity in fish. Dev Comp Immunol 39(1–2):72–78

    Article  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Natural Science Foundation of China [31772870] and the Central Nonprofit Basic Scientific Research Project for the Scientific Research Institutes of China [2420–2019].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiming Peng.

Ethics declarations

Conflict of interest

We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Q., Zeng, J., Wang, Y. et al. Alternations in the liver metabolome, skin and serum antioxidant function of silver pomfret (Pampus Argenteus) is induced by jellyfish feeding. 3 Biotech 11, 192 (2021). https://doi.org/10.1007/s13205-021-02702-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-021-02702-1

Keywords

Navigation