Chitinase; Growth; Gut microbiota; Hermetia illucens; Oreochromis niloticus; Fatty Acids; Chitinases; Fatty Acids, Unsaturated; Animals; Larva; Animal Feed/analysis; Vegetables; Cichlids; Diptera/chemistry; Animal Feed; Diptera; Medicine (miscellaneous); Nutrition and Dietetics
Abstract :
[en] The aim of this study is to determine to what extent the addition of chitinase to black soldier fly (BSF) larval meal enriched or not with long-chain PUFA (LC-PUFA) could improve growth, protein digestion processes and gut microbial composition in Nile tilapia. Two different types of BSF meal were produced, in which larvae were reared on substrates formulated with vegetable culture substrate (VGS) or marine fish offal substrate (FOS). The BSF raised on VGS was enriched in α-linolenic acid (ALA), while that raised on FOS was enriched in ALA + EPA + DHA. Six BSF-based diets, enriched or not with chitinase, were formulated and compared with a control diet based on fishmeal and fish oil (FMFO). Two doses (D) of chitinase from Aspergillus niger (2 g and 5 g/kg feed) were added to the BSF larval diets (VGD0 and FOD0) to obtain four additional diets: VGD2, VGD5, FOD2 and FOD5. After 53 d of feeding, results showed that the BSF/FOS-based diets induced feed utilisation, protein efficiency and digestibility, as well as growth comparable to the FMFO control diet, but better than the BSF/VGS-based diets. The supplementation of chitinase to BSF/FOS increased in fish intestine the relative abundance of beneficial microbiota such as those of the Bacillaceae family. The results showed that LC-PUFA-enriched BSF meal associated with chitinase could be used as an effective alternative to fishmeal in order to improve protein digestion processes, beneficial microbiota and ultimately fish growth rate.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Agbohessou, Pamphile S ; Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium ; Laboratory of Hydrobiology and Aquaculture (LHA), Faculty of Agronomics Sciences (FSA), University of Abomey-Calavi (UAC), Cotonou, Benin
Mandiki, Robert; Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium
Mes, Wouter; Department of Microbiology, Radboud Institute for Biological and Ecological Sciences (RIBES), Radboud University, Nijmegen, the Netherlands
Blanquer, Aude ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Gérardy, Mazarine ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie spéciale et autopsies
Garigliany, Mutien-Marie ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie générale et autopsies
Lambert, Jérôme; Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium
Cambier, Pierre; Unit of Research in Plant Cellular and Molecular Biology, Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium
Tokpon, Nicole; Laboratory of Hydrobiology and Aquaculture (LHA), Faculty of Agronomics Sciences (FSA), University of Abomey-Calavi (UAC), Cotonou, Benin
Lalèyè, Philippe A; Laboratory of Hydrobiology and Aquaculture (LHA), Faculty of Agronomics Sciences (FSA), University of Abomey-Calavi (UAC), Cotonou, Benin
Kestemont, Patrick ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) ; Research Unit in Environmental and Evolutionary Biology (URBE), Institute of Life, Earth and Environment (ILEE), University of Namur, Namur, Belgium
Language :
English
Title :
Effect of fatty acid-enriched black soldier fly larvae meal combined with chitinase on the metabolic processes of Nile tilapia.
The authors thank the \u2018Academie de Recherche et d\u2019Enseignement Sup\u00E9rieur\u2019 (ARES \u2013 CCD, Belgium) for its financial support (accession numbers: 31382).
Hossain MS, Fawole FJ, Labh SN, et al. (2021) Insect meal inclusion as a novel feed ingredient in soy-based diets improves performance of rainbow trout (Oncorhynchus mykiss). Aquaculture 544, 737096. https://doi.org/10.1016/j.aquaculture.2021.737096
Gougbedji A, Detilleux J, Lalèyè P, et al. (2022) Can insect meal replace fishmeal? A meta-analysis of the effects of black soldier fly on fish growth performances and nutritional values. Animals 12, 1700. https://doi.org/10.3390/ani12131700
Zulkifli NFNM, Seok-Kian AY, Seng LL, et al. (2022) Nutritional value of black soldier fly (Hermetia illucens) larvae processed by different methods. PLoS One 17, e0263924. https://doi.org/10.1371/journal.pone.0263924
Hua K (2021) A meta-analysis of the effects of replacing fish meals with insect meals on growth performance of fish. Aquaculture 530, 735732. https://doi.org/10.1016/j.aquaculture.2020.735732
Devic E, Leschen W, Murray F, et al. (2018) Growth performance, feed utilization and body composition of advanced nursing Nile tilapia (Oreochromis niloticus) fed diets containing Black Soldier Fly (Hermetia illucens) larvae meal. Aquacult Nutr 24, 416–423. https://doi.org/10.1111/anu.12573
Agbohessou PS, Mandiki SNM, Gougbédji A, et al. (2021) Efficiency of fatty acid-enriched dipteran-based meal on husbandry, digestive activity and immunological responses of Nile tilapia Oreochromis niloticus juveniles. Aquaculture 545, 737193. https://doi.org/10.1016/j.aquaculture.2021.737193
Ewald N, Vidakovic A, Langeland M, et al. (2020) Fatty acid composition of black soldier fly larvae (Hermetia illucens) – possibilities and limitations for modification through diet. Waste Manag 102, 40–47. https://doi.org/10.1016/j.wasman.2019.10.014
Mohan K, Rajan DK, Muralisankar T, et al. (2022) Use of black soldier fly (Hermetia illucens L.) larvae meal in aquafeeds for a sustainable aquaculture industry: a review of past and future needs. Aquaculture 553, 738095. https://doi.org/10.1016/j.aquaculture.2022.738095
Belghit I, Liland NS, Waagbø R, et al. (2018) Potential of insect-based diets for Atlantic salmon (Salmo salar). Aquaculture 491, 72–81. https://doi.org/10.1016/j.aquaculture.2018.03.016
Ojha S, Bekhit AE-D, Grune T, et al. (2021) Bioavailability of nutrients from edible insects. Curr Opin Food Sci 41, 240–248. https://doi.org/10.1016/j.cofs.2021.08.003
Shiau SY & Yu YP (1999) Dietary supplementation of chitin and chitosan depresses growth in tilapia, Oreochromis niloticus X O. aureus. Aquaculture 179, 439–446. https://doi.org/10.1016/S0044-8486(99)00177-5
Guerreiro I, Serra CR, Coutinho F, et al. (2021) Digestive enzyme activity and nutrient digestibility in meagre (Argyrosomus regius) fed increasing levels of black soldier fly meal (Hermetia illucens). Aquacult Nutr 27, 142–152. https://doi.org/10.1111/anu.13172
Zhang Y, Feng S, Chen J, et al. (2012) Stimulatory effects of chitinase on growth and immune defense of orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol 32, 844–854. https://doi.org/10.1016/j.fsi.2012.02.009
Hasan I, Rimoldi S, Saroglia G, et al. (2023) Sustainable fish feeds with insects and probiotics positively affect freshwater and marine fish gut microbiota. Animals 13, 1633. https://doi.org/10.3390/ani13101633
Weththasinghe P, Rocha SDC, Øyås O, et al. (2022) Modulation of Atlantic salmon (Salmo salar) gut microbiota composition and predicted metabolic capacity by feeding diets with processed black soldier fly (Hermetia illucens) larvae meals and fractions. Anim Microbiome 4, 9. https://doi.org/10.1186/s42523-021-00161-w
Rimoldi S, Antonini M, Gasco L, et al. (2021) Intestinal microbial communities of rainbow trout (Oncorhynchus mykiss) may be improved by feeding a Hermetia illucens meal/low-fishmeal diet. Fish Physiol Biochem 47, 365–380. https://doi.org/10.1007/s10695-020-00918-1
Foysal MJ & Gupta SK (2022) A systematic meta-analysis reveals enrichment of Actinobacteria and Firmicutes in the fish gut in response to black soldier fly (Hermetica illucens) meal-based diets. Aquaculture 549, 737760. https://doi.org/10.1016/j.aquaculture.2021.737760
Falcinelli S, Picchietti S, Rodiles A, et al. (2015) Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism. Sci Rep 5, 9336. https://doi.org/10.1038/srep09336
Banavar A, Amirkolaei SK, Duscher L, et al. (2022) Nutritional evaluation of black soldier fly frass as an ingredient in Florida pompano (Trachinotus carolinus L.) Diets. Animals 12, 2407. https://doi.org/10.3390/ani12182407
Janssen RH, Vincken J-P, van den Broek LAM, et al. (2017) Nitrogen-to-protein conversion factors for three edible insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens. J Agric Food Chem 65, 2275–2278. https://doi.org/10.1021/acs.jafc.7b00471
Kirk PL (1950) Kjeldahl method for total nitrogen. Anal Chem 22, 354–358. https://doi.org/10.1021/ac60038a038
Agbohessou PS, Mandiki SNM, Gougbédji A, et al. (2021) Total replacement of fish meal by enriched-fatty acid Hermetia illucens meal did not substantially affect growth parameters or innate immune status and improved whole body biochemical quality of Nile tilapia juveniles. Aquacult Nutr 27, 880–896. https://doi.org/10.1111/anu.13232
Bessey OA, Lowry OH & Brock MJ (1946) A method for the rapid determination of alkaline phosphates with five cubic millimeters of serum. J Biol Chem 164, 321–329. http://www.ncbi.nlm.nih.gov/pubmed/20989492
Maroux S, Louvard D & Barath J (1973) The aminopeptidase from hog intestinal brush border. Biochim Biophys Acta – Enzymol 321, 282–295. https://doi.org/10.1016/0005-2744 (73)90083-1
Gisbert E, Giménez G, Fernández I, et al. (2009) Development of digestive enzymes in common dentex Dentex dentex during early ontogeny. Aquaculture 287, 381–387. https://doi.org/10.1016/j.aquaculture.2008.10.039
Bernfeld P (1951) Enzymes of starch degradation and synthesis. Adv Enzymol Relat Areas Mol Biol 12, 379–428.
Cuvier-Péres A & Kestemont P (2001) Development of some digestive enzymes in Eurasian perch larvae Perca fluviatilis. Fish Physiol Biochem 24, 279–285. https://doi.org/10.1023/A: 1015033300526
Kakizaki H, Ikeda M, Fukushima H, et al. (2015) Distribution of chitinolytic enzymes in the organs and cDNA cloning of chitinase lsozymes from the stomach of two species of fish, chub mackerel (Scomber japonicus) and silver croaker (Pennahia argentata). Open J Mar Sci 05, 398–411. https://doi.org/10.4236/ojms.2015.54032
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Agbohessou PS, Mandiki SNM, Mbondo Biyong SR, et al. (2022) Intestinal histopathology and immune responses following Escherichia coli lipopolysaccharide challenge in Nile tilapia fed enriched black soldier fly larval (BSF) meal supplemented with chitinase. Fish Shellfish Immunol 128, 620–633. https://doi.org/10.1016/j.fsi.2022.08.050
Fastrès A, Canonne MA, Taminiau B, et al. (2020) Analysis of the lung microbiota in dogs with Bordetella bronchiseptica infection and correlation with culture and quantitative polymerase chain reaction. Vet Res 51, 46. https://doi.org/10.1186/s13567-020-00769-x
Quast C, Pruesse E, Yilmaz P, et al. (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41, D590–D596. https://doi.org/10.1093/nar/gks1219
Kumar S, Stecher G, Li M, et al. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547–1549. https://doi.org/10.1093/molbev/msy096
Furukawa A & Tsukahara H (1966) On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Nippon Suisan Gakkaishi 32, 502–506. https://doi.org/10.2331/suisan.32.502
McMurdie PJ & Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217. https://doi.org/10.1371/journal.pone.0061217
Segata N, Izard J, Waldron L, et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12, R60. https://doi.org/10.1186/gb-2011-12-6-r60
Cornet V, Ouaach A, Mandiki SNM, et al. (2018) Environmentally-realistic concentration of cadmium combined with polyunsaturated fatty acids enriched diets modulated non-specific immunity in rainbow trout. Aquat Toxicol 196, 104–116. https://doi.org/10.1016/j.aquatox.2018.01.012
Arenas M, Álvarez-González A, Barreto Á, et al. (2021) Evaluation of protein: lipid ratio on growth, feed efficiency, and metabolic response in juvenile yellowtail snapper Ocyurus chrysurus (Bloch, 1791). Lat Am J Aquat Res 49, 329–341. https://doi.org/10.3856/vol49-issue2-fulltext-2660
Gutowska MA, Drazen JC & Robison BH (2004) Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp Biochem Physiol – A Mol Integr Physiol 139, 351–358. https://doi.org/10.1016/j.cbpb.2004.09.020
Gohi B, Zeng H-Y & Pan A (2016) Optimization and characterization of chitosan enzymolysis by pepsin. Bioeng 3, 17. https://doi.org/10.3390/bioengineering3030017
Molinari LM, Pedroso RB & de Oliveira Scoaris D, et al. (2007) Identification and partial characterisation of a chitinase from Nile tilapia, Oreochromis niloticus. Comp Biochem Physiol - B Biochem Mol Biol 146, 81–87. https://doi.org/10.1016/j.cbpb.2006.09.004
Karasov WH & Hume ID (1997) Vertebrate gastrointestinal system. In Handbook of Comparative Physiology, pp. 409–480 [W Dantzler, editor]. Bethesda, MD: American Physiological Society. https://doi.org/10.1002/cphy.cp130107
Zarantoniello M, Randazzo B, Truzzi C, et al. (2019) A six-months study on Black Soldier Fly (Hermetia illucens) based diets in zebrafish. Sci Rep 9, 8598. https://doi.org/10.1038/s41598-019-45172-5
Hender A, Siddik M, Howieson J, et al. (2021) Black soldier fly, Hermetia illucens as an alternative to fishmeal protein and fish oil: impact on growth, immune response, mucosal barrier status, and flesh quality of juvenile barramundi, Lates calcarifer (Bloch, 1790). Biology (Basel) 10, 505. https://doi.org/10.3390/biology10060505
Ghanbari M, Kneifel W & Domig KJ (2015) A new view of the fish gut microbiome: advances from next-generation sequencing. Aquaculture 448, 464–475. https://doi.org/10.1016/j.aquaculture.2015.06.033
Orellana LH, Francis TB, Ferraro M, et al. (2022) Verrucomicrobiota are specialist consumers of sulfated methyl pentoses during diatom blooms. ISME J 16, 630–641. https://doi.org/10.1038/s41396-021-01105-7
Ran C, Huang L, Liu Z, et al. (2015) A comparison of the beneficial effects of live and heat-inactivated baker’s yeast on Nile tilapia: suggestions on the role and function of the secretory metabolites released from the yeast. PLoS One 10, e0145448. https://doi.org/10.1371/journal.pone.0145448
Tachibana L, Telli GS, Dias DD, et al. (2021) Bacillus subtilis and Bacillus licheniformis in diets for Nile tilapia (Oreochromis niloticus): effects on growth performance, gut microbiota modulation and innate immunology. Aquac Res 52, 1630–1642. https://doi.org/10.1111/are.15016
Terova G, Gini E, Gasco L, et al. (2021) Effects of full replacement of dietary fishmeal with insect meal from Tenebrio molitor on rainbow trout gut and skin microbiota. J Anim Sci Biotechnol 12, 30. https://doi.org/10.1186/s40104-021-00551-9
Terova G, Rimoldi S, Ascione C, et al. (2019) Rainbow trout (Oncorhynchus mykiss) gut microbiota is modulated by insect meal from Hermetia illucens prepupae in the diet. Rev Fish Biol Fish 29, 465–486. https://doi.org/10.1007/s11160-019-09558-y
Huyben D, Vidaković A, Werner Hallgren S, et al. (2019) High-throughput sequencing of gut microbiota in rainbow trout (Oncorhynchus mykiss) fed larval and pre-pupae stages of black soldier fly (Hermetia illucens). Aquaculture 500, 485–491. https://doi.org/10.1016/j.aquaculture.2018.10.034
Ringø E, Hoseinifar SH, Ghosh K, et al. (2018) Lactic acid bacteria in finfish. Front Microbiol 9, 1818. https://doi.org/10.3389/fmicb.2018.01818
Lin Y-H & Cheng M-Y (2017) Effects of dietary organic acid supplementation on the growth, nutrient digestibility and intestinal histology of the giant grouper Epinephelus lanceolatus fed a diet with soybean meal. Aquaculture 469, 106–111. https://doi.org/10.1016/j.aquaculture.2016.11.032
Askarian F, Zhou Z, Olsen RE, et al. (2012) Culturable autochthonous gut bacteria in Atlantic salmon (Salmo salar L.) fed diets with or without chitin. Characterization by 16S rRNA gene sequencing, ability to produce enzymes and in vitro growth inhibition of four fish pathogens. Aquaculture 326–329, 1–8. https://doi.org/10.1016/j.aquaculture.2011.10.016
Borrelli L, Coretti L, Dipineto L, et al. (2017) Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens. Sci Rep 7, 16269. https://doi.org/10.1038/s41598-017-16560-6
Apper E, Weissman D, Respondek F, et al. (2016) Hydrolysed wheat gluten as part of a diet based on animal and plant proteins supports good growth performance of Asian seabass (Lates calcarifer), without impairing intestinal morphology or microbiota. Aquaculture 453, 40–48. https://doi.org/10.1016/j.aquaculture.2015.11.018
Rimoldi S, Gliozheni E, Ascione C, et al. (2018) Effect of a specific composition of short- and medium-chain fatty acid 1-Monoglycerides on growth performances and gut microbiota of gilthead sea bream (Sparus aurata). PeerJ 6, e5355. https://doi.org/10.7717/peerj.5355
Huyben D, Roehe BK, Bekaert M, et al. (2020) Dietary lipid: protein ratio and n-3 long-chain polyunsaturated fatty acids alters the gut microbiome of Atlantic salmon under hypoxic and normoxic conditions. Front Microbiol 11, 589898. https://doi.org/10.3389/fmicb.2020.589898
Ingerslev H-C, von Gersdorff Jørgensen L, Lenz Strube M, et al. (2014) The development of the gut microbiota in rainbow trout (Oncorhynchus mykiss) is affected by first feeding and diet type. Aquaculture 424–425, 24–34. https://doi.org/10.1016/j.aquaculture.2013.12.032