A Diet Rich in HUFAs Enhances the Energetic and Immune Response Capacities of Larvae of the Scallop Argopecten purpuratus

Simple Summary Scallop aquaculture depends on hatchery-reared larvae that frequently present mass mortalities due to bacterial infections. Herein, it was demonstrated that the administration of a diet based on microalgae rich in omega 3 increases larval cell membrane fluidity and energy metabolic capacity, which in turn enhances immune capacity and resistance to bacterial infection. Additionally, this diet enhances larval growth and survival; thus, its application would be a promising strategy for improving scallop aquaculture productivity. Abstract Massive mortalities in farmed larvae of the scallop Argopecten purpuratus have been associated with pathogenic Vibrio outbreaks. An energetic trade-off between development-associated demands and immune capacity has been observed. Given that highly unsaturated fatty acids (HUFAs) are essential nutrients for larval development, we evaluated the effect of diets based on microalgae low and high in HUFAs (LH and HH, respectively) on the energetic condition and the immune response of scallop larvae. The results showed that the HH diet increased cellular membrane fluidity in veliger larvae. The routine respiration rate was 64% higher in the HH-fed veligers than in the LH-fed veligers. Additionally, the metabolic capacity tended to be higher in the HH-fed veligers than in the LH-fed veligers after the Vibrio challenge. After the challenge, the HH-fed veligers presented higher transcript induction of ApTLR (immune receptor) and ApGlys (immune effector) genes, and the HH-fed pediveligers presented higher induction of ApLBP/BPI1 (antimicrobial immune effector) gene, than the LH-fed larvae. Furthermore, the HH-fed veligers controlled total Vibrio proliferation (maintaining near basal levels) after the bacterial challenge, while the LH-fed veligers were not able to control this proliferation, which increased three-fold. Finally, the HH-fed larvae showed 20–25% higher growth and survival rates than the LH-fed veligers. Overall, the results indicated that the administration of a HH diet increases cell membrane fluidity and energy metabolic capacity, which in turn enhances immunity and the ability to control Vibrio proliferation. The administration of microalgae high in HUFAs would be a promising strategy for improving scallop larval production efficiency.

[1]  K. Brokordt,et al.  Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response , 2023, Frontiers in Immunology.

[2]  J. Barja,et al.  First Report, Characterization and Pathogenicity of Vibrio chagasii Isolated from Diseased Reared Larvae of Chilean Scallop, Argopecten purpuratus (Lamarck, 1819) , 2023, Pathogens.

[3]  L. Mercado,et al.  A g-type lysozyme from the scallop Argopecten purpuratus participates in the immune response and in the stability of the hemolymph microbiota. , 2022, Fish & shellfish immunology.

[4]  K. Brokordt,et al.  Metabolic Cost of the Immune Response During Early Ontogeny of the Scallop Argopecten purpuratus , 2021, Frontiers in Physiology.

[5]  L. Mercado,et al.  Expression of immune-related genes during early development of the scallop Argopecten purpuratus after Vibrio splendidus challenge , 2020 .

[6]  Q. Gao,et al.  Metabolomic and transcriptomic profiling reveals the alteration of energy metabolism in oyster larvae during initial shell formation and under experimental ocean acidification , 2020, Scientific Reports.

[7]  F. Bosco,et al.  The Potential for Natural Antioxidant Supplementation in the Early Stages of Neurodegenerative Disorders , 2020, International journal of molecular sciences.

[8]  Patrick Mair,et al.  Robust statistical methods in R using the WRS2 package , 2020, Behavior research methods.

[9]  K. Brokordt,et al.  Molecular characterization and expression patterns of two LPS binding /bactericidal permeability-increasing proteins (LBP/BPIs) from the scallop Argopecten purpuratus. , 2019, Fish & shellfish immunology.

[10]  C. Lodeiros,et al.  Experimental cultures of giant lion s paw Nodipecten subnodosus in equatorial waters of the eastern Pacific: progress in larval development and suspended culture , 2019, Latin American Journal of Aquatic Research.

[11]  M. Doherty,et al.  Lipidomics analysis of juveniles’ blue mussels (Mytilus edulis L. 1758), a key economic and ecological species , 2019, bioRxiv.

[12]  L. Mercado,et al.  Reproduction Immunity Trade-Off in a Mollusk: Hemocyte Energy Metabolism Underlies Cellular and Molecular Immune Responses , 2019, Front. Physiol..

[13]  Qing Wang,et al.  Lipid Structure and Composition Control Consequences of Interleaflet Coupling in Asymmetric Vesicles. , 2018, Biophysical journal.

[14]  L. Mercado,et al.  Molecular characterization and protein localization of the antimicrobial peptide big defensin from the scallop Argopecten purpuratus after Vibrio splendidus challenge , 2017, Fish & shellfish immunology.

[15]  M. Galdiero,et al.  Microbial Diseases of Bivalve Mollusks: Infections, Immunology and Antimicrobial Defense , 2017, Marine drugs.

[16]  J. Santander,et al.  First Report of Vibrio tubiashii Associated with a Massive Larval Mortality Event in a Commercial Hatchery of Scallop Argopecten purpuratus in Chile , 2016, Front. Microbiol..

[17]  K. Brokordt,et al.  A diet rich in polyunsaturated fatty acids improves the capacity for HSP70 synthesis in adult scallop Argopecten purpuratus and their offspring , 2016 .

[18]  T. Coba de la Peña,et al.  Molecular characterization of two ferritins of the scallop Argopecten purpuratus and gene expressions in association with early development, immune response and growth rate. , 2016, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[19]  L. Mercado,et al.  Molecular characterization of an inhibitor of NF-κB in the scallop Argopecten purpuratus: First insights into its role on antimicrobial peptide regulation in a mollusk. , 2016, Fish & shellfish immunology.

[20]  J. Romalde,et al.  Vibrio bivalvicida sp. nov., a novel larval pathogen for bivalve molluscs reared in a hatchery. , 2016, Systematic and applied microbiology.

[21]  K. Brokordt,et al.  Reproduction reduces HSP70 expression capacity in Argopecten purpuratus scallops subject to hypoxia and heat stress , 2015 .

[22]  Doris Oliva,et al.  Effect of stocking density and food ration on growth and survival of veliger and pediveliger larvae of the taquilla clam Mulinia edulis reared in the laboratory , 2014 .

[23]  Taro Kawai,et al.  Toll-Like Receptor Signaling Pathways , 2014, Front. Immunol..

[24]  C. Miranda,et al.  Effect of florfenicol and oxytetracycline treatments on the intensive larval culture of the Chilean scallop Argopecten purpuratus (Lamarck, 1819) , 2013 .

[25]  Yingying Gao,et al.  Nutrient deprivation enhances lipid content in marine microalgae. , 2013, Bioresource technology.

[26]  Huan Zhang,et al.  Identification and characterisation of pathogenic Vibrio splendidus from Yesso scallop (Patinopecten yessoensis) cultured in a low temperature environment. , 2013, Journal of invertebrate pathology.

[27]  Mengqiang Wang,et al.  The expression of immune-related genes during the ontogenesis of scallop Chlamys farreri and their response to bacterial challenge. , 2013, Fish & shellfish immunology.

[28]  I. Martínez‐Pita,et al.  Biochemical and energy dynamics during larval development of the mussel Mytilus galloprovincialis (Lamarck, 1819) , 2012 .

[29]  R. Boushel,et al.  Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects , 2012, The Journal of physiology.

[30]  P. Boudry,et al.  Expression of candidate genes related to metabolism, immunity and cellular stress during massive mortality in the American oyster Crassostrea virginica larvae in relation to biochemical and physiological parameters. , 2012, Gene.

[31]  Y. Marty,et al.  Diet and performance in the scallop, Argopecten purpuratus: force production during escape responses and mitochondrial oxidative capacities , 2011 .

[32]  V. Coyne,et al.  The importance of ATP in the immune system of molluscs , 2011 .

[33]  R. Tremblay,et al.  Lipid requirements of the scallop Pecten maximus (L.) during larval and post-larval development in relation to addition of Rhodomonas salina in diet , 2010 .

[34]  M. Hellberg,et al.  A new lysozyme from the eastern oyster, Crassostrea virginica, and a possible evolutionary pathway for i-type lysozymes in bivalves from host defense to digestion , 2010, BMC Evolutionary Biology.

[35]  Vorrapon Chaikeeratisak,et al.  Proteomic analysis of differentially expressed proteins in Penaeus monodon hemocytes after Vibrio harveyi infection , 2010, Proteome Science.

[36]  R. Robert,et al.  Effect of nutrition on Crassostrea gigas larval development and the evolution of physiological indices. Part A: Quantitative and qualitative diet effects , 2010 .

[37]  Guy Duportail,et al.  Monitoring biophysical properties of lipid membranes by environment-sensitive fluorescent probes. , 2009, Biophysical journal.

[38]  E. Uribe,et al.  A comparison of larval production of the northern scallop, Argopecten purpuratus, in closed and recirculating culture systems , 2009 .

[39]  G. C. Zittelli,et al.  Pavlova lutheri: Production, preservation and use as food for Crassostrea gigas larvae , 2008 .

[40]  A. Beaumont,et al.  The effect of microalgal diets on growth, biochemical composition, and fatty acid profile of Crassostrea corteziensis (Hertlein) juveniles , 2007 .

[41]  M. Garnier,et al.  Evidence for the Involvement of Pathogenic Bacteria in Summer Mortalities of the Pacific Oyster Crassostrea gigas , 2007, Microbial Ecology.

[42]  J. Xiang,et al.  Effect of stocking density on growth, settlement and survival of clam larvae, Meretrix meretrix , 2006 .

[43]  Zhi Wang,et al.  Isolation of Vibrio parahaemolyticus from abalone (Haliotis diversicolor supertexta L.) postlarvae associated with mass mortalities , 2006 .

[44]  V. Bricelj,et al.  Lipid class dynamics during larval ontogeny of sea scallops, Placopecten magellanicus, in relation to metamorphic success and response to antibiotics , 2006 .

[45]  C. Parrish,et al.  Effect of varying dietary levels of ω6 polyunsaturated fatty acids during the early ontogeny of the sea scallop , 2005 .

[46]  M. Houde,et al.  Phagocytosis: the convoluted way from nutrition to adaptive immunity , 2005, Immunological reviews.

[47]  D. Roff,et al.  An analysis of trade‐offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus , 2005 .

[48]  A. J. Hulbert,et al.  Dietary fats and membrane function: implications for metabolism and disease , 2005, Biological reviews of the Cambridge Philosophical Society.

[49]  R. Tremblay,et al.  Effect of varying levels of dietary essential fatty acid during early ontogeny of the sea scallop Placopecten magellanicus , 2004 .

[50]  L. Milke,et al.  Growth of postlarval sea scallops, Placopecten magellanicus, on microalgal diets, with emphasis on the nutritional role of lipids and fatty acids , 2004 .

[51]  J. G. Bell,et al.  Polyunsaturated fatty acids in total lipid and phospholipids of chilean scallop Argopecten purpuratus (L.) larvae: effects of diet and temperature , 2003 .

[52]  I. Hirono,et al.  Characterization and function of kuruma shrimp lysozyme possessing lytic activity against Vibrio species. , 2003, Gene.

[53]  A. J. Hulbert,et al.  Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease states and metabolism , 2003, Naturwissenschaften.

[54]  P. Soudant,et al.  Effect of a mono-specific algal diet on immune functions in two bivalve species - Crassostrea gigas and Ruditapes philippinarum , 2003, Journal of Experimental Biology.

[55]  D. Lemos,et al.  Citrate synthase and pyruvate kinase activities during early life stages of the shrimp Farfantepenaeus paulensis (Crustacea, Decapoda, Penaeidae): effects of development and temperature. , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[56]  A. Patrzykat,et al.  Gone gene fishing: how to catch novel marine antimicrobials. , 2003, Trends in biotechnology.

[57]  P. Sorgeloos,et al.  Effect of lipid emulsions on production and fatty acid composition of eggs of the scallop Argopecten purpuratus , 2003 .

[58]  M. Auffret,et al.  Changes in circulating and tissue-infiltrating hemocyte parameters of European flat oysters, Ostrea edulis, naturally infected with Bonamia ostreae. , 2003, Journal of invertebrate pathology.

[59]  R. Tremblay,et al.  Variation of lipid class and fatty acid composition of Chaetoceros muelleri and Isochrysis sp. grown in a semicontinuous system , 2003 .

[60]  G. Sorci,et al.  Trade-off between immunocompetence and growth in magpies: an experimental study , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  J. Navarro,et al.  Effect of three conditioning diets on the fatty acid composition of gonads and muscle of Argopecten purpuratus , 2002 .

[62]  Alexander D. MacKerell,et al.  Polyunsaturated fatty acids in lipid bilayers: intrinsic and environmental contributions to their unique physical properties. , 2002, Journal of the American Chemical Society.

[63]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[64]  V. Bricelj,et al.  Physiological basis for energy demands and early postlarval mortality in the Pacific oyster, Crassostrea gigas , 2001 .

[65]  R. Hancock,et al.  Synergistic Interactions between Mammalian Antimicrobial Defense Peptides , 2001, Antimicrobial Agents and Chemotherapy.

[66]  H. Godfray,et al.  Basis of the trade–off between parasitoid resistance and larval competitive ability in Drosophila melanogaster , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  K. Brokordt,et al.  Effect of reproduction on escape responses and muscle metabolic capacities in the scallop Chlamys islandica Müller 1776. , 2000, Journal of experimental marine biology and ecology.

[68]  P. Sorgeloos,et al.  The Chilean scallop Argopecten purpuratus (Lamarck, 1819): I. fatty acid composition and lipid content of six organs , 1999 .

[69]  P. Soudant,et al.  Fatty acid composition of polar lipid classes during larval development of scallop Pecten maximus (L.) , 1998 .

[70]  J. Castilla,et al.  A biochemical study of the larval and postlarval stages of the Chilean scallop Argopecten purpuratus , 1998 .

[71]  A. Maeda-Martínez,et al.  Ingestion and digestion index of catarina scallop Argopecten ventricosus-circularis, Sowerby II, 1842, veliger larvae with ten microalgae species , 1997 .

[72]  C. Riquelme,et al.  Bacteriology of the scallop Argopecten purpuratus (Lamarck, 1819) cultured in Chile , 1995 .

[73]  C. Riquelme,et al.  Pathogenicity studies on a Vibrio anguillarum-related (VAR) strain causing an epizootic in Argopecten purpuratus larvae cultured in Chile , 1995 .

[74]  E. Gratton,et al.  Membrane lipid domains and dynamics as detected by Laurdan fluorescence , 1995, Journal of Fluorescence.

[75]  Y. Marty,et al.  The effect of monospecific algal diets on growth and fatty acid composition of Pecten maximus (L.) larvae , 1993 .

[76]  Y. Marty,et al.  Changes in the fatty acid composition of Pecten maximus (L.) during larval development , 1992 .

[77]  Y. Marty,et al.  Growth and lipid class composition of Pecten maximus (L.) larvae grown under hatchery conditions , 1992 .

[78]  A. Gawlicka,et al.  Qualitative modification of muscle metabolic organization with thermal acclimation of rainbow trout, Oncorhynchus mykiss , 1992, Fish Physiology and Biochemistry.

[79]  P. Calder,et al.  Uptake and incorporation of saturated and unsaturated fatty acids into macrophage lipids and their effect upon macrophage adhesion and phagocytosis. , 1990, The Biochemical journal.

[80]  B. Macdonald Physiological energetics of Japanese scallop Patinopecten yessoensis larvae , 1988 .

[81]  C. Langdon,et al.  The effect of algal and artificial diets on the growth and fatty acid composition of Crassostrea gigas Spat , 1981, Journal of the Marine Biological Association of the United Kingdom.

[82]  Javier Gómez-León,et al.  CRECIMIENTO Y SUPERVIVENCIA DE LARVAS DE ARGOPECTEN NUCLEUS ALIMENTADAS CON DIFERENTES DIETAS MICROALGALES , 2016 .

[83]  Rafael Opazo,et al.  Characterization and pathogenicity of Vibrio splendidus strains associated with massive mortalities of commercial hatchery-reared larvae of scallop Argopecten purpuratus (Lamarck, 1819). , 2015, Journal of invertebrate pathology.

[84]  Thorsten Dickhaus,et al.  Simultaneous Statistical Inference , 2014, Springer Berlin Heidelberg.

[85]  Tiz iana Parasass Membrane Lipid Domains and Dynamics as Detected by Laurdan Fluorescence , 2004 .

[86]  M. Sprung Physiological energetics of mussel larvae (Mytiius edulis). III. Respiration , 1984 .

[87]  M. Sprung,et al.  Physiological energetics of mussel larvae (Mytilus edulis). II. Food uptake , 1984 .

[88]  W. Smith,et al.  Culture of Marine Invertebrate Animals , 1975, Springer US.

[89]  F. Smith,et al.  COLORIMETRIC METHOD FOR DETER-MINATION OF SUGAR AND RELATED SUBSTANCE , 1956 .

[90]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .