Skip to main content

Advertisement

Log in

Metabolic profiling of mussel larvae: effect of handling and culture conditions

  • European Aquaculture Development since 1993
  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Gas chromatography mass spectroscopy was applied to characterize the metabolic profiles of hatchery-reared mussel (Perna canaliculus) larvae before and after a prolonged handling and water exchange process, and to investigate the effect of culture conditions. A decrease in succinate and an increase in alanine were observed after the water exchange, which indicated alterations in energy production and osmotic balance. However, these variations were subtle and it is unlikely that the water exchange practice had any lasting negative effects on larval physiology and performance. Multivariate pattern recognition tools (hierarchical clustering, principal component analysis and projection to latent squares discriminant analysis) were used to assess metabolite variations in larvae reared in low-density static and high-density flow through systems and to construct a culture condition classification model. Twelve metabolites contributed most towards the model, which indicated differences in energy, protein and lipid metabolism. The clear group separations were not represented by observable variations in morphological traits. This suggests that growth performance is metabolically buffered through an adaptive physiological mechanism to provide similar developmental characteristics under these conditions.

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

Similar content being viewed by others

References

  • Aggio R, Villas-Bôas SG, Ruggiero K (2011) Metab: an R package for high-throughput analysis of metabolomics data generated by GC-MS. Bioinformatics 27:2316–2318

    Article  CAS  PubMed  Google Scholar 

  • Alfaro AC, Young T (in review) Showcasing metabolomics in aquaculture: a review. Aquac Rev

  • Anestis A, Pörtner HO, Michaelidis B (2010) Anaerobic metabolic patterns related to stress responses in hypoxia exposed mussels Mytilus galloprovincialis. J Exp Mar Biol Ecol 394(1):123–133

    Article  CAS  Google Scholar 

  • Capson TL, Guinotte J (2014) Future proofing New Zealand’s shellfish aquaculture: monitoring and adaptation to ocean acidification. New Zealand Aquatic Environment and Biodiversity Report, No. 136, Ministry for Primary Industries. ISBN 978-0-478-43763-8

  • Carrasco AV, Astorga M, Cisterna A, Farías A, Espinoza V, Uriarte I (2014) Pre-feasibility study for the installation of a Chilean mussel Mytilus chilensis (Hupé, 1854) seed hatchery in the Lakes region, Chile. Fish Aquac J 5(3):102. doi:10.4172/2150-3508.1000102

    Google Scholar 

  • Carregosa V, Figueira E, Gil AM, Pereira S, Pinto J, Soares AM, Freitas R (2014) Tolerance of Venerupis philippinarum to salinity: osmotic and metabolic aspects. Comp Biochem Physiol A Mol Integr Physiol 171:36–43

    Article  CAS  PubMed  Google Scholar 

  • Connor KM, Gracey AY (2012) High-resolution analysis of metabolic cycles in the intertidal mussel Mytilus californianus. Am J Physiol-Regul Integr Comp Physiol 302(1):R103–R111

    Article  CAS  PubMed  Google Scholar 

  • Deaton L (2009) Osmotic and ionic regulation in molluscs. In: Evan DH (ed) Osmotic and ionic regulations: cells and animals. CRC Press, Boca Raton, pp 107–133

    Google Scholar 

  • Dunphy BJ, Watts E, Ragg NL (2015) Identifying thermally-stressed adult green-lipped mussels (Perna canaliculus Gmelin, 1791) via metabolomic profiling. Am Malacol Bull 33(1):1–9

    Article  Google Scholar 

  • Hanana H, Simon G, Kervarec N, Cérantola S (2014) Evaluation of toxicological effects induced by tributyltin in clam Ruditapes decussatus using high-resolution magic angle spinning nuclear magnetic resonance spectroscopy: study of metabolic responses in heart tissue and detection of a novel metabolite. Toxicol Rep 1:777–786

    Article  CAS  Google Scholar 

  • Ji C, Wu H, Wei L, Zhao J, Wang Q, Lu H (2013) Responses of Mytilus galloprovincialis to bacterial challenges by metabolomics and proteomics. Fish Shellfish Immunol 35(2):489–498

    Article  CAS  PubMed  Google Scholar 

  • Ji C, Cao L, Li F (2015) Toxicological evaluation of two pedigrees of clam Ruditapes philippinarum as bioindicators of heavy metal contaminants using metabolomics. Environ Toxicol Pharmacol 39(2):545–554

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Tian LX, Xie SW, Guo DQ, Yang HJ, Liang GY, Liu YJ (2015) Interactions between dietary protein levels, growth performance, feed utilization, gene expression and metabolic products in juvenile grass carp (Ctenopharyngodon idella). Aquaculture 437:75–83

    Article  CAS  Google Scholar 

  • Kamermans P, Galley T, Boudry P, Fuentes J, Mccombie H, Batista FM, Blanco A, Dominguez L, Cornette F, Pincot L, Beaumont A (2013) Blue mussel hatchery technology in Europe. In Allan G, Burnell G (eds) Advances in aquaculture hatchery technology. Woodhead Publishing series in food science, technology and nutrition, pp 339–373

  • Karakach TK, Huenupi EC, Soo EC, Walter JA, Afonso LO (2009) 1H-NMR and mass spectrometric characterization of the metabolic response of juvenile Atlantic salmon (Salmo salar) to long-term handling stress. Metabolomics 5(1):123–137

    Article  CAS  Google Scholar 

  • Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2012a) Performance of single and multi-strain probiotics during hatchery production of Greenshell™ mussel larvae, Perna canaliculus. Aquaculture 354–355:56–63

    Article  Google Scholar 

  • Kesarcodi-Watson A, Miner P, Nicolas JL, Robert R (2012b) Protective effect of four potential probiotics against pathogen-challenge of the larvae of three bivalves: pacific oyster (Crassostrea gigas), flat oyster (Ostrea edulis) and scallop (Pecten maximus). Aquaculture 344–349:29–34

    Article  Google Scholar 

  • Koyama H, Okamoto S, Watanabe N, Hoshino N, Jimbo M, Yasumoto K, Watabe S (2015) Dynamic changes in the accumulation of metabolites in brackish water clam Corbicula japonica associated with alternation of salinity. Comp Biochem Physiol B Biochem Mol Biol 181:59–70

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Dong B, Tang B, Zhang T, Xiang J (2006) Effect of stocking density on growth, settlement and survival of clam larvae Meretrix meretrix. Aquaculture 258(1):344–349

    Article  Google Scholar 

  • Liu CC, Shin PKS, Cheung SG (2014) Comparisons of the metabolic responses of two subtidal nassariid gastropods to hypoxia and re-oxygenation. Mar Pollut Bull 82(1):109–116

    Article  CAS  PubMed  Google Scholar 

  • Martell DJ, Duhaime J, Parsons GJ (2013) Proof of concept of a scalable hatchery system using modular principles to increase production and survival for commercially important Mytilus species. In: Canadian Aquaculture R&D Review 2013 (p 57). Aquaculture Association of Canada Special Publication 23

  • Patti GJ, Yanes O, Siuzdak G (2012) Innovation: metabolomics: the apogee of the omics trilogy. Nat Rev Mol Cell Biol 13(4):263–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ragg NL, King N, Watts E, Morrish J (2010) Optimising the delivery of the key dietary diatom Chaetoceros calcitrans to intensively cultured Greenshell™ mussel larvae, Perna canaliculus. Aquaculture 306(1–4):270–280

    Article  Google Scholar 

  • Ralston-Hooper KJ, Adamec J, Jannash A, Mollenhauer R, Ochoa-Acuña H, Sepúlveda MS (2011) Use of GC × GC/TOF-MS and LC/TOF-MS for metabolomic analysis of Hyalella aztecachronically exposed to atrazine and its primary metabolite, desethylatrazine. J Appl Toxicol 31(5):399–410

    Article  CAS  PubMed  Google Scholar 

  • Roznere I, Watters GT, Wolfe BA, Daly M (2014) Nontargeted metabolomics reveals biochemical pathways altered in response to captivity and food limitation in the freshwater mussel Amblema plicata. Comp Biochem Physiol D Genom Proteom 12:53–60

    CAS  Google Scholar 

  • Schock TB, Duke J, Goodson A, Weldon D, Brunson J, Leffler JW, Bearden DW (2013) Evaluation of Pacific white shrimp (Litopenaeus vannamei) health during a superintensive aquaculture growout using NMR-based metabolomics. PLoS One 8(3):e59521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scottish Aquaculture Research Forum (SARF) 2014. New approaches to Mussel Seedstock acquisition. Final report, contract reference: SARF096. ISBN: 978-1-907266-62-1

  • Smart KF, Aggio RB, Van Houtte JR, Villas-Bôas SG (2010) Analytical platform for metabolome analysis of microbial cells using MCF derivatization followed by gas chromatography-mass spectrometry. Nat Protoc 5:1709–1729

    Article  CAS  PubMed  Google Scholar 

  • Spann N, Aldridge DC, Griffin JL, Jones OA (2011) Size-dependent effects of low level cadmium and zinc exposure on the metabolome of the Asian clam, Corbicula fluminea. Aquat Toxicol 105(3):589–599

    Article  CAS  PubMed  Google Scholar 

  • Tuffnail W, Mills GA, Cary P, Greenwood R (2009) An environmental 1H NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation. Metabolomics 5(1):33–43

    Article  CAS  Google Scholar 

  • Villas-Bôas SG, Nielsen J, Smedsgaard J, Hansen MA, Roessner-Tunali U (2007) Metabolome analysis: an introduction. Wiley, New Jersey, p 319. ISBN: 978-0-471-74344-6

  • Villas-Bôas SG, Smart KF, Sivakumaran S, Lane GA (2011) Alkylation or silylation for analysis of amino and non-amino organic acids by GC-MS? Metabolites 1:3–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson J (2008) Mussel seed supply—are hatcheries part of the solution? Shellfish News 25:16–19

    Google Scholar 

  • Wu H, Ji C, Wang Q, Liu X, Zhao J, Feng J (2013a) Manila clam Venerupis philippinarum as a biomonitor to metal pollution. Chin J Oceanol Limnol 31(1):65–74

    Article  CAS  Google Scholar 

  • Wu H, Ji C, Wei L, Zhao J, Lu H (2013b) Proteomic and metabolomic responses in hepatopancreas of Mytilus galloprovincialis challenged by Micrococcus luteus and Vibrio anguillarum. J Proteom 94:54–67

    Article  CAS  Google Scholar 

  • Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucl Acids Res 43(W1):W251–W257

    Article  PubMed  PubMed Central  Google Scholar 

  • Young T, Alfaro AC (in review) A primer for metabolomics research in aquaculture. Aquac Rev

  • Young T, Alfaro AC, Robertson J (2011) Effect of neuroactive compounds on the settlement of mussel (Perna canaliculus) larvae. Aquaculture 319(1):277–283

    Article  CAS  Google Scholar 

  • Young T, Alfaro AC, Sánchez-Lazo C, Robertson J (2015a) Putative involvement of adrenergic receptors in regulation of mussel (Perna canaliculus) larval settlement. Mar Biol Res (ahead of print): 1–11. doi:10.1080/17451000.2014.979833

  • Young T, Alfaro AC, Villas-Bôas S (2015b) Identification of candidate biomarkers for quality assessment of hatchery-reared mussel larvae via GC/MS-based metabolomics. NZ J Mar Freshwat Res 49(1):87–95

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are thankful to Rodney Roberts, Dan McCall, Nicola Hawes, Sarah Cumming and Shellfish Production and Technology New Zealand Ltd (SPATnz) for assisting with larval production, and to Margarita Markovskaya for assistance with the sample processing at the Metabolomics Laboratory, University of Auckland. We also thank Kathy Campbell for editorial corrections that improved this manuscript. This project was partially funded by a Faculty Research Grant to A. C. Alfaro. We are grateful for the fruitful discussions with the Aquaculture Biotechnology Group, which improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea C. Alfaro.

Additional information

Guest editors: Elena Mente and Aad Smaal/European Aquaculture Development since 1993: The benefits of aquaculture to Europe and the perspectives of European aquaculture production.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Young, T., Alfaro, A.C. & Villas-Bôas, S.G. Metabolic profiling of mussel larvae: effect of handling and culture conditions. Aquacult Int 24, 843–856 (2016). https://doi.org/10.1007/s10499-015-9945-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-015-9945-0

Keywords

Navigation