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Transcriptomic assessment of dietary fishmeal partial replacement by soybean meal and prebiotics inclusion in the liver of juvenile Pacific yellowtail (Seriola lalandi)

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Abstract

Background

Seriola lalandi is an important species for aquaculture, due to its rapid growth, adaptation to captivity and formulated diets, and high commercial value. Due to the rise in fishmeal (FM) price, efforts have been and still are made to replace it partially or entirely with vegetable meals in diets for carnivorous fish. The use of prebiotics when feeding vegetable meals has improved fish health.

Methods

Four experimental diets were assessed in juveniles, the control diet consisted of FM as the main protein source, the second diet included 2% of GroBiotic®-A (FM-P), in the third diet FM was partially replaced (25%) by soybean meal (SM25), and the fourth consisted of SM25 with 2% of GroBiotic®-A (SM25-P). Growth was evaluated and RNA-seq of the liver tissue was performed, including differential expression analysis and functional annotation to identify genes affected by the diets.

Results

Growth was not affected by this level of FM replacement, but it was improved by prebiotics. Annotation was achieved for 59,027 transcripts. Gene expression was affected by the factors: 225 transcripts due to FM replacement, 242 due to prebiotics inclusion, and 62 due to the interaction of factors. The SM25-P diet showed the least amount of differentially expressed genes against the control diet.

Conclusion

The replacement of FM (25%) by soybean meal combined with prebiotics (2%) represents a good cost-benefit balance for S. lalandi juveniles since the fish growth increased and important metabolic and immune system genes in the liver were upregulated with this diet.

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Data availability

All the RNA-Seq raw reads were deposited into the Sequencing Read Archive (SRA) of NCBI with the accession number SRR10211853 to SRR10211864. The BioProject ID of our data is PRJNA575250 and the BioSample accession is SAMN12816772.

References

  1. Abbink W, Blanco Garcia A, Roques JAC et al (2012) The effect of temperature and pH on the growth and physiological response of juvenile yellowtail kingfish Seriola lalandi in recirculating aquaculture systems. Aquaculture 330–333:130–135. https://doi.org/10.1016/j.aquaculture.2011.11.043

    Article  CAS  Google Scholar 

  2. Avilés A, Castelló F (2004) Manual para el Cultivo de Seriola lalandi en Baja California sur México Jurel. Instituto Nacional de la Pesca, Mexico City

    Google Scholar 

  3. Ottolenghi F, Silvestri C, Giordano P et al (2004) Capture-based aquaculture: the fattening of eels, groupers, tunas and yellowtails. FAO, Rome

    Google Scholar 

  4. Gomon M (2008) Fishes of Australia’s southern coast. Reed New Holland, Museum Victoria, Chatswood

    Google Scholar 

  5. Nugroho E, Ferrell DJ, Smith P, Taniguchi N (2001) Genetic divergence of kingfish from Japan, Australia and New Zealand inferred by microsatellite DNA and mitochondrial DNA control region markers. Fish Sci 67:843–850. https://doi.org/10.1046/j.1444-2906.2001.00331.x

    Article  CAS  Google Scholar 

  6. Symonds JE, Walker SP, Pether S et al (2014) Developing yellowtail kingfish (Seriola lalandi) and ha¯puku (Polyprion oxygeneios) for New Zealand aquaculture. New Zeal J Mar Freshw Res 48:371–384

    Article  CAS  Google Scholar 

  7. Riddick EW (2013) Insect protein as a partial replacement for fishmeal in the diets of juvenile fish and crustaceans. Mass production of beneficial organisms: invertebrates and entomopathogens. Elsevier Inc., Amsterdam, pp 565–582

    Google Scholar 

  8. Kubiriza GK (2018) A review of conventional and unconventional feeds in fish nutrition. Aquac Nutr 24:703–708. https://doi.org/10.3382/ps.0601905

    Article  Google Scholar 

  9. Shannon L, Waller L (2021) A cursory look at the fishmeal/oil industry from an ecosystem perspective. Front Ecol Evol 9:1–9. https://doi.org/10.3389/fevo.2021.645023

    Article  Google Scholar 

  10. Gatlin DM, Barrows FT, Brown P et al (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579

    Article  CAS  Google Scholar 

  11. Oliva-Teles A, Enes P, Peres H (2015) Replacing fishmeal and fish oil in industrial aquafeeds for carnivorous fish. Feed and feeding practices in aquaculture. Elsevier, Amsterdam, pp 203–233

    Chapter  Google Scholar 

  12. Chakraborty P, Mallik A, Sarang N, Lingam SS (2019) A review on alternative plant protein sources available for future sustainable aqua feed production. Int J Chem Stud 7:1399–1404

    CAS  Google Scholar 

  13. Hodar AR, Vasava R, Mahavadiya DR, Joshi NH (2020) Fish meal and fish oil replacement for aqua feed formulation by using alternative sources: a review. J Exp Zool India 23:13–21

    Google Scholar 

  14. Kader MA, Bulbul M, Koshio S et al (2012) Effect of complete replacement of fishmeal by dehulled soybean meal with crude attractants supplementation in diets for red sea bream, Pagrus major. Aquaculture 350–353:109–116. https://doi.org/10.1016/j.aquaculture.2012.04.009

    Article  CAS  Google Scholar 

  15. Makkar HPS (1993) Antinutritional factors in foods for livestock. BSAP Occas Publ 16:69–85. https://doi.org/10.1017/s0263967x00031086

    Article  Google Scholar 

  16. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    Article  CAS  Google Scholar 

  17. Iwashita Y, Yamamoto T, Furuita H et al (2008) Influence of certain soybean antinutritional factors supplemented to a casein-based semipurified diet on intestinal and liver morphology in fingerling rainbow trout Oncorhynchus mykiss. Fish Sci 74:1075–1082. https://doi.org/10.1111/j.1444-2906.2008.01627.x

    Article  CAS  Google Scholar 

  18. Burr G, Hume M, Neill WH, Gatlin DM (2008) Effects of prebiotics on nutrient digestibility of a soybean-meal-based diet by red drum Sciaenops ocellatus (Linnaeus). Aquac Res 39:1680–1686. https://doi.org/10.1111/j.1365-2109.2008.02044.x

    Article  CAS  Google Scholar 

  19. Li P, Gatlin DM (2004) Dietary brewers yeast and the prebiotic GrobioticTM AE influence growth performance, immune responses and resistance of hybrid striped bass (Morone chrysops x M. saxatilis) to Streptococcus iniae infection. Aquaculture 231:445–456. https://doi.org/10.1016/j.aquaculture.2003.08.021

    Article  Google Scholar 

  20. Li P, Gatlin DM (2005) Evaluation of the prebiotic GroBiotic®-A and brewers yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops x M. saxatilis) challenged in situ with Mycobacterium marinum. Aquaculture. Elsevier, Amsterdam, pp 197–205

    Google Scholar 

  21. Song SK, Beck BR, Kim D et al (2014) Prebiotics as immunostimulants in aquaculture: a review. Fish Shellfish Immunol 40:40–48

    Article  CAS  PubMed  Google Scholar 

  22. Gatlin DM (2015) Prebiotics. Dietary nutrients, additives, and fish health. Wiley, Hoboken, pp 271–281

    Chapter  Google Scholar 

  23. Guerreiro I, Oliva-Teles A, Enes P (2018) Prebiotics as functional ingredients: focus on Mediterranean fish aquaculture. Rev Aquac 10:800–832

    Article  Google Scholar 

  24. Manning TS, Gibson GR (2004) Prebiotics. Best Pract Res Clin Gastroenterol 18:287–298

    Article  PubMed  Google Scholar 

  25. Dalmo RA, Bøgwald J (2008) ß-Glucans as conductors of immune symphonies. Fish Shellfish Immunol 25:384–396

    Article  CAS  PubMed  Google Scholar 

  26. Delzenne NM (2003) Oligosaccharides: state of the art. Proc Nutr Soc 62:177–182. https://doi.org/10.1079/PNS2002225

    Article  CAS  PubMed  Google Scholar 

  27. Delzenne NM, Williams CM (2002) Prebiotics and lipid metabolism. Curr Opin Lipidol 13:61–67. https://doi.org/10.1097/00041433-200202000-00009

    Article  CAS  PubMed  Google Scholar 

  28. Baanante IV, Garcia de Frutos P, Bonamusa L, Fernandez F (1991) Regulation of fish glycolysis—gluconeogenesis: role of fructose 2,6 P2 and PFK-2. Comp Biochem Physiol Part B 100:11–17. https://doi.org/10.1016/0305-0491(91)90077-Q

    Article  Google Scholar 

  29. Metón I, Mediavilla D, Caseras A et al (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis–gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82:223–232. https://doi.org/10.1017/S0007114599001403

    Article  PubMed  Google Scholar 

  30. Morais S, Pratoomyot J, Taggart JB et al (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genomics 12:1–17. https://doi.org/10.1186/1471-2164-12-255

    Article  CAS  Google Scholar 

  31. Goto T, Takagi S, Ichiki T et al (2001) Studies on the green liver in cultured red sea bream fed low level and non-fish meal diets: relationship between hepatic taurine and biliverdin levels. Fish Sci 67:58–63. https://doi.org/10.1046/j.1444-2906.2001.00199.x

    Article  CAS  Google Scholar 

  32. Peng S, Chen L, Qin JG et al (2008) Effects of replacement of dietary fish oil by soybean oil on growth performance and liver biochemical composition in juvenile black seabream, Acanthopagrus schlegeli. Aquaculture 276:154–161. https://doi.org/10.1016/j.aquaculture.2008.01.035

    Article  CAS  Google Scholar 

  33. Panserat S, Hortopan GA, Plagnes-Juan E et al (2009) Differential gene expression after total replacement of dietary fish meal and fish oil by plant products in rainbow trout (Oncorhynchus mykiss) liver. Aquaculture 294:123–131. https://doi.org/10.1016/j.aquaculture.2009.05.013

    Article  CAS  Google Scholar 

  34. Gille C, Bölling C, Hoppe A et al (2010) HepatoNet1: a comprehensive metabolic reconstruction of the human hepatocyte for the analysis of liver physiology. Mol Syst Biol 6:411. https://doi.org/10.1038/msb.2010.62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Liang XF, Ogata HY, Oku H (2002) Effect of dietary fatty acids on lipoprotein lipase gene expression in the liver and visceral adipose tissue of fed and starved red sea bream Pagrus major. In: Hedrick M (ed) Comparative biochemistry and physiology—a molecular and integrative physiology. Elsevier Inc., Amsterdam, pp 913–919

    Google Scholar 

  36. Craig SR, Washburn BS, Gatlin DM (1999) Effects of dietary lipids on body composition and liver function in juvenile red drum, Sciaenops ocellatus. Fish Physiol Biochem 21:249–255. https://doi.org/10.1023/A:1007843420128

    Article  CAS  Google Scholar 

  37. Ruyter B, Moya-Falcón C, Rosenlund G, Vegusdal A (2006) Fat content and morphology of liver and intestine of Atlantic salmon (Salmo salar): Effects of temperature and dietary soybean oil. Aquaculture 252:441–452. https://doi.org/10.1016/j.aquaculture.2005.07.014

    Article  CAS  Google Scholar 

  38. Farkas T, Csengeri I, Majoros F, Oláh J (1980) Metabolism of fatty acids in fish. III. Combined effect of environmental temperature and diet on formation and deposition of fatty acids in the carp, Cyprinus carpio Linnaeus 1758. Aquaculture 20:29–40. https://doi.org/10.1016/0044-8486(80)90059-9

    Article  CAS  Google Scholar 

  39. Sitjà-Bobadilla A, Peña-Llopis S, Gómez-Requeni P et al (2005) Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 249:387–400. https://doi.org/10.1016/j.aquaculture.2005.03.031

    Article  CAS  Google Scholar 

  40. Zheng X, Tocher DR, Dickson CA et al (2004) Effects of diets containing vegetable oil on expression of genes involved in highly unsaturated fatty acid biosynthesis in liver of Atlantic salmon (Salmo salar). Aquaculture 236:467–483. https://doi.org/10.1016/j.aquaculture.2004.02.003

    Article  CAS  Google Scholar 

  41. Rumsey GL, Kinsella JE, Shetty KJ, Hughes SG (1991) Effect of high dietary concentrations of brewer’s dried yeast on growth performance and liver uricase in rainbow trout (Oncorhynchus mykiss). Anim Feed Sci Technol 33:177–183. https://doi.org/10.1016/0377-8401(91)90058-Z

    Article  Google Scholar 

  42. Mourente G, Bell JG (2006) Partial replacement of dietary fish oil with blends of vegetable oils (rapeseed, linseed and palm oils) in diets for European sea bass (Dicentrarchus labrax L.) over a long term growth study: effects on muscle and liver fatty acid composition and effectiveness of a fish oil finishing diet. Comp Biochem Physiol Part B 145:389–399. https://doi.org/10.1016/j.cbpb.2006.08.012

    Article  CAS  Google Scholar 

  43. Caballero MJ, López-Calero G, Socorro J et al (1999) Combined effect of lipid level and fish meal quality on liver histology of gilthead seabream (Sparus aurata). Aquaculture 179:277–290. https://doi.org/10.1016/S0044-8486(99)00165-9

    Article  CAS  Google Scholar 

  44. Tocher DR, Bell JG, MacGlaughlin P et al (2001) Hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition of liver in salmonids: effects of dietary vegetable oil. Comp Biochem Physiol 130:257–270. https://doi.org/10.1016/S1096-4959(01)00429-8

    Article  CAS  Google Scholar 

  45. Kemski MM, Rappleye CA, Dabrowski K et al (2020) Transcriptomic response to soybean meal-based diets as the first formulated feed in juvenile yellow perch (Perca flavescens). Sci Rep 10:3998. https://doi.org/10.1038/s41598-020-59691-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Xiong Y, Huang J, Li X et al (2014) Deep sequencing of the tilapia (Oreochromis niloticus) liver transcriptome response to dietary protein to starch ratio. Aquaculture 433:299–306. https://doi.org/10.1016/j.aquaculture.2014.06.009

    Article  CAS  Google Scholar 

  47. He S, You JJ, Liang XF et al (2021) Transcriptome sequencing and metabolome analysis of food habits domestication from live prey fish to artificial diets in mandarin fish (Siniperca chuatsi). BMC Genomics 22:129. https://doi.org/10.1186/s12864-021-07403-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Xue X, Hixson SM, Hori TS et al (2015) Atlantic salmon (Salmo salar) liver transcriptome response to diets containing Camelina sativa products. Comp Biochem Physiol Part D 14:1–15. https://doi.org/10.1016/j.cbd.2015.01.005

    Article  CAS  Google Scholar 

  49. Prisingkorn W, Prathomya P, Jakovlić I et al (2017) Transcriptomics, metabolomics and histology indicate that high-carbohydrate diet negatively affects the liver health of blunt snout bream (Megalobrama amblycephala). BMC Genomics 18:856. https://doi.org/10.1186/s12864-017-4246-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Jobling M (2003) The thermal growth coefficient (TGC) model of fish growth: a cautionary note. Aquac Res 34:581–584. https://doi.org/10.1046/j.1365-2109.2003.00859.x

    Article  Google Scholar 

  51. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. https://doi.org/10.1186/1471-2105-12-323

  55. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21. https://doi.org/10.1186/s13059-014-0550-8

    Article  CAS  Google Scholar 

  56. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  57. Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/index.html

  58. Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  60. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57. https://doi.org/10.1038/nprot.2008.211

    Article  CAS  Google Scholar 

  61. Bowyer JN, Qin JG, Smullen RP et al (2013) The use of a soy product in juvenile yellowtail kingfish (Seriola lalandi) feeds at different water temperatures: 2. Soy protein concentrate. Aquaculture 410–411:1–10. https://doi.org/10.1016/j.aquaculture.2013.06.001

    Article  CAS  Google Scholar 

  62. Bowyer JN, Qin JG, Smullen RP et al (2013) The use of a soy product in juvenile yellowtail kingfish (Seriola lalandi) feeds at different water temperatures: 1. Solvent extracted soybean meal. Aquaculture 384–387:35–45. https://doi.org/10.1016/j.aquaculture.2012.12.005

    Article  CAS  Google Scholar 

  63. Jirsa D, Davis A, Stuart K, Drawbridge M (2011) Development of a practical soy-based diet for California yellowtail, Seriola lalandi. Aquac Nutr 17:e869–e874. https://doi.org/10.1111/j.1365-2095.2011.00856.x

    Article  Google Scholar 

  64. Stone DAJ, Bellgrove EJ, Forder REA et al (2018) Inducing subacute enteritis in yellowtail kingfish Seriola lalandi: the effect of dietary inclusion of soybean meal and grape seed extract on hindgut morphology and inflammation. N Am J Aquac 80:59–68. https://doi.org/10.1002/naaq.10002

    Article  Google Scholar 

  65. Gahr SA, Weber GM, Rexroad CE (2012) Identification and expression of Smads associated with TGF-β/activin/nodal signaling pathways in the rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:1233–1244. https://doi.org/10.1007/s10695-012-9611-7

    Article  CAS  PubMed  Google Scholar 

  66. Yoshida GM, Lhorente JP, Carvalheiro R, Yáñez JM (2017) Bayesian genome-wide association analysis for body weight in farmed Atlantic salmon (Salmo salar L.). Anim Genet 48:698–703. https://doi.org/10.1111/age.12621

    Article  CAS  PubMed  Google Scholar 

  67. Du J, Chen X, Wang J et al (2019) Comparative skin transcriptome of two Oujiang color common carp (Cyprinus carpio var. color) varieties. Fish Physiol Biochem 45:177–185. https://doi.org/10.1007/s10695-018-0551-8

    Article  CAS  PubMed  Google Scholar 

  68. Rasal KD, Shah TM, Vaidya M et al (2015) Analysis of consequences of non-synonymous SNP in feed conversion ratio associated TGF-β receptor type 3 gene in chicken. Meta Gene 4:107–117. https://doi.org/10.1016/j.mgene.2015.03.006

    Article  PubMed  PubMed Central  Google Scholar 

  69. Seiliez I, Gabillard JC, Skiba-Cassy S et al (2008) An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol 295:329–335. https://doi.org/10.1152/ajpregu.00146.2008

    Article  CAS  Google Scholar 

  70. Wu C, Okar DA, Newgard CB, Lange AJ (2001) Overexpression of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase in mouse liver lowers blood glucose by suppressing hepatic glucose production. J Clin Invest 107:91–98. https://doi.org/10.1172/JCI11103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Metón I, Caseras A, Fernández F, Baanante IV (2000) 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene expression is regulated by diet composition and ration size in liver of gilthead sea bream, Sparus aurata. Biochim Biophys Acta 1491:220–228. https://doi.org/10.1016/S0167-4781(00)00040-3

    Article  PubMed  Google Scholar 

  72. Clarke JL, Mason PJ (2003) Murine hexose-6-phosphate dehydrogenase: a bifunctional enzyme with broad substrate specificity and 6-phosphogluconolactonase activity. Arch Biochem Biophys 415:229–234. https://doi.org/10.1016/S0003-9861(03)00229-7

    Article  CAS  PubMed  Google Scholar 

  73. Kotaka M, Gover S, Vandeputte-Rutten L et al (2005) Structural studies of glucose-6-phosphate and NADP+ binding to human glucose-6-phosphate dehydrogenase. Acta Crystallogr Sect D Biol Crystallogr 61:495–504. https://doi.org/10.1107/S0907444905002350

    Article  CAS  Google Scholar 

  74. Printen JA, Brady MJ, Saltiel AR (1997) PTG, a protein phosphate 1-binding protein with a role in glycogen metabolism. Science 275:1475–1478. https://doi.org/10.1126/science.275.5305.1475

    Article  CAS  PubMed  Google Scholar 

  75. Urs S, Smith C, Campbell B et al (2004) Gene expression profiling in human preadipocytes and adipocytes by microarray analysis. J Nutr 134:762–770. https://doi.org/10.1093/jn/134.4.762

    Article  CAS  PubMed  Google Scholar 

  76. Onat OE, Gulsuner S, Bilguvar K et al (2013) Missense mutation in the ATPase, aminophospholipid transporter protein ATP8A2 is associated with cerebellar atrophy and quadrupedal locomotion. Eur J Hum Genet 21:281–285. https://doi.org/10.1038/ejhg.2012.170

    Article  CAS  PubMed  Google Scholar 

  77. Jaye M, Lynch KJ, Krawiec J et al (1999) A novel endothelial-derived lipase that modulates HDL metabolism. Nat Genet 21:424–428. https://doi.org/10.1038/7766

    Article  CAS  PubMed  Google Scholar 

  78. Gropler MC, Harris TE, Hall AM et al (2009) Lipin 2 is a liver-enriched phosphatidate phosphohydrolase enzyme that is dynamically regulated by fasting and obesity in mice. J Biol Chem 284:6763–6772. https://doi.org/10.1074/jbc.M807882200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Leduc A, Zatylny-Gaudin C, Robert M et al (2018) Dietary aquaculture by-product hydrolysates: impact on the transcriptomic response of the intestinal mucosa of European seabass (Dicentrarchus labrax) fed low fish meal diets. BMC Genomics 19:396. https://doi.org/10.1186/s12864-018-4780-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39:223–239

    Article  CAS  Google Scholar 

  81. Dudkina NV, Spicer BA, Reboul CF et al (2016) Structure of the poly-C9 component of the complement membrane attack complex. Nat Commun 7:1–6. https://doi.org/10.1038/ncomms10588

    Article  CAS  Google Scholar 

  82. Fu YW, Zhu CK, Zhang QZ, Hou TL (2019) Molecular characterization, expression analysis, and ontogeny of complement component C9 in southern catfish (Silurus meridionalis). Fish Shellfish Immunol 86:449–458. https://doi.org/10.1016/j.fsi.2018.11.069

    Article  CAS  PubMed  Google Scholar 

  83. Guo B, Wu C, Lv Z, Liu C (2016) Characterisation and expression analysis of two terminal complement components: C7 and C9 from large yellow croaker, Larimichthys crocea. Fish Shellfish Immunol 51:211–219. https://doi.org/10.1016/j.fsi.2016.01.015

    Article  CAS  PubMed  Google Scholar 

  84. Alper CA, Abramson N, Johnston RB et al (1970) Studies in vivo and in vitro on an abnormality in the metabolism of C3 in a patient with increased susceptibility to infection. J Clin Invest 49:1975–1985. https://doi.org/10.1172/JCI106417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was carried out thanks to the support of the Mexican National Council for Science and Technology (CONACYT). The co-author Rigoberto Delgado-Vega thanks for the Ph.D. scholarship and Denisse Chávez-García for the Master’s scholarship, both granted by CONACYT.

Funding

This work was funded by the Consejo Nacional de Ciencia y Tecnología (CONACYT, México) through the Centro de Investigación Científica y Educación Superior de Ensenada, Baja California (CICESE) internal projects 682136 and 623159.

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Authors and Affiliations

  1. Department of Marine Biotechnology, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana #3918, Zona Playitas, 22860, Ensenada, Baja California, México

    Oscar E. Juárez, Edgar López-Landavery & Clara Elizabeth Galindo-Sánchez

  2. Department of Aquaculture, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana #3918, Zona Playitas, 22860, Ensenada, Baja California, México

    Fabiola Lafarga-De la Cruz, Juan Pablo Lazo, Rigoberto Delgado-Vega & Denisse Chávez-García

  3. Aquaculture Program, Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Av. Instituto Politécnico Nacional #195, Playa Palo de Santa Rita Sur, 23096, La Paz, Baja California Sur, México

    Dariel Tovar-Ramírez

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  1. Oscar E. Juárez
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OEJ: Conceptualization, Formal analysis, Visualization, Writing—original draft. FLDC: Conceptualization, Methodology, Resources, Supervision, Writing—review and editing. JPL: Conceptualization, Methodology, Investigation, Resources, Funding acquisition, Supervision, Writing—review and editing. RDV: Data curation, Formal analysis, Writing—original draft. DCG: Investigation, Data curation, Formal analysis. ELL: Data curation, Formal analysis, Writing—review and editing. DTR: Conceptualization, Methodology, Supervision, Writing—review and editing. CEGS: Conceptualization, Methodology, Resources, Funding acquisition, Supervision, Writing—review and editing.

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Correspondence to Clara Elizabeth Galindo-Sánchez.

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This research complied with the Guidelines of the European Union Council (2010/63/EU) and the Mexican Government (NOM-062—ZOO-1999) for the production, care, and use of experimental animals, and with the ARRIVE guidelines. The protocols used in this work were approved by the Bioethics Committee of the Centro de Investigación Científica y de Educación Superior de Ensenada, Baja California (CICESE).

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Juárez, O.E., Lafarga-De la Cruz, F., Lazo, J.P. et al. Transcriptomic assessment of dietary fishmeal partial replacement by soybean meal and prebiotics inclusion in the liver of juvenile Pacific yellowtail (Seriola lalandi). Mol Biol Rep 48, 7127–7140 (2021). https://doi.org/10.1007/s11033-021-06703-4

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