Hermetia illucens larvae as a Fishmeal replacement alters intestinal specific bacterial populations and immune homeostasis in weanling piglets.

Hermetia illucens larvae meal (HILM) are rich in proteins and chitin, and represent an innovative feed ingredient for animals. However, little is known about the intestinal bacteria and immune homeostasis response of HILM as a fishmeal replacement on weanling piglets. Thus, this study aimed to investigate the changes in specific ileal and cecal bacterial populations and their metabolic profiles, and ileal immune indexes in weanling piglets fed with a diet containing HILM. A total of 128 weanling piglets were fed either a basal diet or 1 of 3 diets with 1%, 2%, and 4% HILM (HI0, HI1, HI2, and HI4, respectively). Each group consisted of 8 pens (replicates), with 4 pigs per pen. After 28 d of feeding, 8 barrows per treatment were euthanized, the ileal and cecal digesta, and ileal mucosa were collected for analyzing bacterial population and metabolic profiles, and immune indexes, respectively. Results showed that HILM increased (P < 0.05, maximum in HI2) the number of Lactobacillus and Bifidobacterium in the ileum and cecum, but quadratically decreased (P < 0.05, minimum in HI2) the number of Escherichia coli. In the cecum, the number of Firmicutes, Ruminococcus, Clostridium cluster IV, and Prevotella showed a quadratic response to increasing (P < 0.05, maximum in HI2) HILM levels. Lactate and butyrate concentrations in the ileum and cecum were quadratically increased (P < 0.05, maximum in HI2) with increasing HILM levels. In the cecum, the amines, phenol, and indole compounds concentrations were quadratically decreased (P < 0.05, minimum in HI2) with increasing HILM levels, while total short-chain fatty acids and acetate concentrations were quadratically increased (P < 0.05, maximum in HI2). In the ileum, the TLR4, NF-κB, MyD88, and TNF-α mRNA expressions were quadratically decreased (P < 0.05, minimum in HI2) with increasing HILM levels, while the mRNA expression of IL-10, barrier function (MUC1, ZO-1, Occludin, and Claudin-2), and development-related genes (IGF-1, GLP-2, and EGF) was quadratically increased (P < 0.05, maximum in HI2). Furthermore, the changes in the mucosal gene expression were associated with changes in the bacterial populations and their metabolites. Collectively, these results showed that a diet supplemented with 2% HILM affected specific bacterial populations and metabolic profiles, and maintained ileal immune status. These findings provide new insights into the use of insect meal as a suitable alternative protein source for swine feeding.

[1]  Gang Wang,et al.  Use of Hermetia illucens larvae as a dietary protein source: Effects on growth performance, carcass traits, and meat quality in finishing pigs. , 2019, Meat science.

[2]  Gang Wang,et al.  Hermetia illucens larvae as a potential dietary protein source altered the microbiota and modulated mucosal immune status in the colon of finishing pigs , 2019, Journal of Animal Science and Biotechnology.

[3]  Gang Wang,et al.  Microbiome-Metabolomics Analysis Investigating the Impacts of Dietary Starch Types on the Composition and Metabolism of Colonic Microbiota in Finishing Pigs , 2019, Front. Microbiol..

[4]  H. M. Munang'andu,et al.  Gut health and vaccination response in pre‐smolt Atlantic salmon (Salmo salar) fed black soldier fly (Hermetia illucens) larvae meal , 2019, Fish & shellfish immunology.

[5]  D. Huyben,et al.  High-throughput sequencing of gut microbiota in rainbow trout (Oncorhynchus mykiss) fed larval and pre-pupae stages of black soldier fly (Hermetia illucens) , 2019, Aquaculture.

[6]  S. Wesselingh,et al.  Opportunistic bacteria confer the ability to ferment prebiotic starch in the adult cystic fibrosis gut , 2018, Gut microbes.

[7]  M. Capucchio,et al.  Influence of Hermetia illucens meal dietary inclusion on the histological traits, gut mucin composition and the oxidative stress biomarkers in rainbow trout (Oncorhynchus mykiss) , 2018, Aquaculture.

[8]  Weiyun Zhu,et al.  Effects of Intravenous Infusion With Sodium Butyrate on Colonic Microbiota, Intestinal Development- and Mucosal Immune-Related Gene Expression in Normal Growing Pigs , 2018, Front. Microbiol..

[9]  Weiyun Zhu,et al.  Caecal infusion of the short‐chain fatty acid propionate affects the microbiota and expression of inflammatory cytokines in the colon in a fistula pig model , 2018, Microbial biotechnology.

[10]  Yun-mi Kim,et al.  Black soldier fly (Hermetia illucens) larvae enhances immune activities and increases survivability of broiler chicks against experimental infection of Salmonella Gallinarum , 2018, The Journal of veterinary medical science.

[11]  L. Bruni,et al.  Characterisation of the intestinal microbial communities of rainbow trout (Oncorhynchus mykiss) fed with Hermetia illucens (black soldier fly) partially defatted larva meal as partial dietary protein source , 2018 .

[12]  Yuguang Du,et al.  Chitin Oligosaccharide Modulates Gut Microbiota and Attenuates High-Fat-Diet-Induced Metabolic Syndrome in Mice , 2018, Marine drugs.

[13]  M. Eeckhout,et al.  Gut antimicrobial effects and nutritional value of black soldier fly (Hermetia illucens L.) prepupae for weaned piglets , 2018 .

[14]  L. Dipineto,et al.  Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens , 2017, Scientific Reports.

[15]  C. Mu,et al.  Long-term effects of early antibiotic intervention on blood parameters, apparent nutrient digestibility, and fecal microbial fermentation profile in pigs with different dietary protein levels , 2017, Journal of Animal Science and Biotechnology.

[16]  M. Capucchio,et al.  Evaluation of the suitability of a partially defatted black soldier fly (Hermetia illucens L.) larvae meal as ingredient for rainbow trout (Oncorhynchus mykiss Walbaum) diets , 2017, Journal of Animal Science and Biotechnology.

[17]  Jehee Lee,et al.  Metagenomics analysis of gut microbiota and immune modulation in zebrafish (Danio rerio) fed chitosan silver nanocomposites , 2017, Fish & shellfish immunology.

[18]  Zan Huang,et al.  Increases in circulating amino acids with in-feed antibiotics correlated with gene expression of intestinal amino acid transporters in piglets , 2017, Amino Acids.

[19]  E. Zoetendal,et al.  Differences in Microbiota Membership along the Gastrointestinal Tract of Piglets and Their Differential Alterations Following an Early-Life Antibiotic Intervention , 2017, Front. Microbiol..

[20]  D. Berry,et al.  Microbial nutrient niches in the gut , 2017, Environmental microbiology.

[21]  R. Olsen,et al.  The effect of dietary chitin on growth and nutrient digestibility in farmed Atlantic cod, Atlantic salmon and Atlantic halibut , 2017 .

[22]  Weiyun Zhu,et al.  Microbiome-metabolome analysis reveals unhealthy alterations in the composition and metabolism of ruminal microbiota with increasing dietary grain in a goat model. , 2016, Environmental microbiology.

[23]  C. Mu,et al.  Bromochloromethane, a Methane Analogue, Affects the Microbiota and Metabolic Profiles of the Rat Gastrointestinal Tract , 2015, Applied and Environmental Microbiology.

[24]  Xiaonan Lu,et al.  Effects of Dietary Lycopene Supplementation on Plasma Lipid Profile, Lipid Peroxidation and Antioxidant Defense System in Feedlot Bamei Lamb , 2015, Asian-Australasian journal of animal sciences.

[25]  G. Bosch,et al.  Insects: a protein-rich feed ingredient in pig and poultry diets , 2015 .

[26]  Gilles Tran,et al.  State-of-the-art on use of insects as animal feed. , 2014 .

[27]  Xiao-qiang Yu,et al.  Insect antimicrobial peptides and their applications , 2014, Applied Microbiology and Biotechnology.

[28]  C. Mu,et al.  Determination of Biogenic Amines in Digesta by High Performance Liquid Chromatography with Precolumn Dansylation , 2014 .

[29]  G. Eudoxie,et al.  Assessing Maturity of Rotary Barrel Green Waste Composts for Use as Tomato and Sweet Pepper Seedling Starter and Transplant Growth Substrates , 2014 .

[30]  E. Weiss,et al.  Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. , 2013, Animal : an international journal of animal bioscience.

[31]  D. Tomé,et al.  Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host. , 2013, Pharmacological research.

[32]  A. Huis Potential of Insects as Food and Feed in Assuring Food Security , 2013 .

[33]  A. Macpherson,et al.  Interactions Between the Microbiota and the Immune System , 2012, Science.

[34]  W. Verstraete,et al.  Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice. , 2012, The Journal of nutritional biochemistry.

[35]  S. Khempaka,et al.  Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers , 2011 .

[36]  C. Abbott,et al.  Growth factor based therapies and intestinal disease: is glucagon-like peptide-2 the new way forward? , 2009, Cytokine & growth factor reviews.

[37]  N. Barnich,et al.  CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. , 2007, The Journal of clinical investigation.

[38]  C. Nyachoti,et al.  Performance responses and indicators of gastrointestinal health in early-weaned pigs fed low-protein amino acid-supplemented diets. , 2006, Journal of animal science.

[39]  M. Marounek,et al.  Susceptibility of Clostridium perfringens to C2–C18 fatty acids , 2005, Letters in applied microbiology.

[40]  F. Shanahan,et al.  Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. , 2005, Gastroenterology.

[41]  M. Roberfroid,et al.  Dietary modulation of the human colonic microbiota: updating the concept of prebiotics , 2004, Nutrition Research Reviews.

[42]  J. Holst,et al.  Supplementation of total parenteral nutrition with butyrate acutely increases structural aspects of intestinal adaptation after an 80% jejunoileal resection in neonatal piglets. , 2004, JPEN. Journal of parenteral and enteral nutrition.

[43]  J. Decuypere,et al.  The combined use of triacylglycerols containing medium-chain fatty acids and exogenous lipolytic enzymes as an alternative to in-feed antibiotics in piglets: concept, possibilities and limitations. An overview , 2003, Nutrition Research Reviews.

[44]  P. Sangild,et al.  Glucagon-Like Peptide 2 Enhances Maltase-Glucoamylase and Sucrase-Isomaltase Gene Expression and Activity in Parenterally Fed Premature Neonatal Piglets , 2002, Pediatric Research.

[45]  H. V. Carey,et al.  Oral IGF-I enhances nutrient and electrolyte absorption in neonatal piglet intestine. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[46]  J. Roth,et al.  The contribution of poly-L-lysine, epidermal growth factor and streptavidin to EGF/PLL/DNA polyplex formation , 1998, Gene Therapy.

[47]  Board on Agriculture,et al.  Nutrient requirements of swine , 1964 .

[48]  A. L. Chaney,et al.  Modified reagents for determination of urea and ammonia. , 1962, Clinical chemistry.