Soya saponins and prebiotics alter intestinal functions in Ballan wrasse (Labrus bergylta)

Abstract A 5-week feeding trial was conducted in the cleaner fish Ballan wrasse (Labrus bergylta) for a better understanding of the basic biology of the intestinal functions and health in this stomach less species. During the trial, Ballan wrasse was fed either a reference diet, the reference diet supplemented with (i) a commercial prebiotic (Aquate™ SG, 0·4 %) expected to have beneficial effects, (ii) soya saponins (0·7 %) expected to induce inflammation or (iii) a combination of the prebiotics and the soya saponins to find a remedy for gut inflammation. Blood, intestinal tissue and gut content from four consecutive intestinal segments (IN1 – IN4) were collected. No significant differences in fish growth were observed between the four dietary groups. Saponin supplementation, both alone and in combination with prebiotics, increased weight index of IN2 and IN3 and decreased blood plasma glucose, cholesterol and total protein. Dry matter of intestinal content and activity of digestive enzymes were not affected by diet. Histomorphological analyses revealed a progressing inflammation with increased infiltration by immune cells particularly into the distal parts of the intestine in fish fed diets with saponins, both alone and in combination with prebiotics. Gene expression profiles obtained by RNA sequencing and quantitative PCR mirrored the histological and biochemical changes induced by the saponin load. The study demonstrated that Ballan wrasse gut health and digestive function may be markedly affected by feed ingredients containing antinutrients.

[1]  T. Kortner,et al.  Digestive and immune functions in the intestine of wild Ballan wrasse (Labrus bergylta). , 2021, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[2]  T. Kortner,et al.  Technical feed quality influences health, digestion patterns, body mineralization and bone development in farming of the stomachless cleaner fish ballan wrasse (Labrus bergylta) , 2021 .

[3]  Ø. Sæle,et al.  Physical and nutrient stimuli differentially modulate gut motility patterns, gut transit rate, and transcriptome in an agastric fish, the ballan wrasse. , 2021, PloS one.

[4]  S. Chi,et al.  Effects of fish meal replacement by low‐gossypol cottonseed meal on growth performance, digestive enzyme activity, intestine histology and inflammatory gene expression of silver sillago ( Sillago sihama Forsskál) (1775) , 2020 .

[5]  R. D. Hatton,et al.  Insulin-Like Growth Factors Are Key Regulators of T Helper 17 Regulatory T Cell Balance in Autoimmunity. , 2020, Immunity.

[6]  X. Leng,et al.  Effects of fish meal replaced by fermented soybean meal on growth performance, intestinal histology and microbiota of largemouth bass ( Micropterus salmoides ) , 2020 .

[7]  I. Hordvik,et al.  Analysis of immunoglobulin and T cell receptor gene expression in ballan wrasse (Labrus bergylta) revealed an extraordinarily high IgM expression in the gut , 2019, Fish & shellfish immunology.

[8]  T. Kortner,et al.  Intestinal Function of the Stomachless Fish, Ballan Wrasse (Labrus bergylta) , 2019, Front. Mar. Sci..

[9]  I. Guerreiro,et al.  Prebiotics as functional ingredients: focus on Mediterranean fish aquaculture , 2018 .

[10]  C. Bain,et al.  Origin, Differentiation, and Function of Intestinal Macrophages , 2018, Front. Immunol..

[11]  L. Stien,et al.  Salmon lice treatments and salmon mortality in Norwegian aquaculture: a review , 2018, Reviews in Aquaculture.

[12]  B. Jabri,et al.  Diverse developmental pathways of intestinal intraepithelial lymphocytes , 2018, Nature Reviews Immunology.

[13]  H. Migaud,et al.  Sustainable production and use of cleaner fish for the biological control of sea lice: recent advances and current challenges , 2018, Veterinary Record.

[14]  Zhiyu Zhang,et al.  Soya‐saponins induce intestinal inflammation and barrier dysfunction in juvenile turbot (Scophthalmus maximus) , 2018, Fish & shellfish immunology.

[15]  T. Marsh,et al.  Effect of dietary prebiotics and probiotics on snakehead (Channa striata) health: Haematology and disease resistance parameters against Aeromonas hydrophila , 2018, Fish & shellfish immunology.

[16]  A. Nederbragt,et al.  Loss of stomach, loss of appetite? Sequencing of the ballan wrasse (Labrus bergylta) genome and intestinal transcriptomic profiling illuminate the evolution of loss of stomach function in fish , 2018, BMC Genomics.

[17]  Marcin Kozak,et al.  What's normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions , 2018 .

[18]  Wei Xu,et al.  Effects of fish meal replacement by soybean meal with supplementation of functional compound additives on intestinal morphology and microbiome of Japanese seabass (Lateolabrax japonicus) , 2017 .

[19]  M. Izquierdo,et al.  Effect of fishmeal and fish oil replacement by vegetable meals and oils on gut health of European sea bass (Dicentrarchus labrax) , 2017 .

[20]  T. Kortner,et al.  Intestinal Fluid Permeability in Atlantic Salmon (Salmo salar L.) Is Affected by Dietary Protein Source , 2016, PloS one.

[21]  M. Øverland,et al.  Dietary Butyrate Helps to Restore the Intestinal Status of a Marine Teleost (Sparus aurata) Fed Extreme Diets Low in Fish Meal and Fish Oil , 2016, PloS one.

[22]  J. Cotton,et al.  Interleukin-8 in gastrointestinal inflammation and malignancy: induction and clinical consequences , 2016 .

[23]  I. Opstad,et al.  Fishmeal quality and ethoxyquin effects on the weaning performance of ballan wrasse (Labrus bergylta) larvae , 2016 .

[24]  I. Opstad,et al.  Marine raw material choice, quality and weaning performance of Ballan wrasse (Labrus bergylta) larvae , 2015 .

[25]  T. Kortner,et al.  Soya Saponins Induce Enteritis in Atlantic Salmon (Salmo salar L.). , 2015, Journal of agricultural and food chemistry.

[26]  M. Izquierdo,et al.  Effects of dietary concentrated mannan oligosaccharides supplementation on growth, gut mucosal immune system and liver lipid metabolism of European sea bass (Dicentrarchus labrax) juveniles. , 2015, Fish & shellfish immunology.

[27]  K. Kaur,et al.  Drug resistance in sea lice: a threat to salmonid aquaculture. , 2015, Trends in parasitology.

[28]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[29]  B. Beck,et al.  Prebiotics as immunostimulants in aquaculture: a review. , 2014, Fish & shellfish immunology.

[30]  T. Kortner,et al.  Effects of dietary phytosterols and soy saponins on growth, feed utilization efficiency and intestinal integrity of gilthead sea bream (Sparus aurata) juveniles , 2014 .

[31]  H. Migaud,et al.  Delousing efficiency of farmed ballan wrasse (Labrus bergylta) against Lepeophtheirus salmonis infecting Atlantic salmon (Salmo salar) post-smolts. , 2014, Pest management science.

[32]  H. Browman,et al.  Wrasse (Labridae) as cleaner fish in salmonid aquaculture – The Hardangerfjord as a case study , 2014 .

[33]  P. Malhotra,et al.  Overactivation of Intestinal SREBP2 in Mice Increases Serum Cholesterol , 2014, PloS one.

[34]  J. Schwartz,et al.  Modulation of autoimmune diseases by interleukin (IL)-17 producing regulatory T helper (Th17) cells , 2013, The Indian journal of medical research.

[35]  T. Kortner,et al.  Effects of dietary plant meal and soya-saponin supplementation on intestinal and hepatic lipid droplet accumulation and lipoprotein and sterol metabolism in Atlantic salmon (Salmo salar L.) , 2013, British Journal of Nutrition.

[36]  H. Browman,et al.  Delousing of Atlantic salmon (Salmo salar) by cultured vs. wild ballan wrasse (Labrus bergylta) , 2013 .

[37]  M. Betancor,et al.  Enhanced intestinal epithelial barrier health status on European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. , 2013, Fish & shellfish immunology.

[38]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[39]  B. Koop,et al.  Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. , 2013, Fish & shellfish immunology.

[40]  Å. Krogdahl,et al.  Transcriptional regulation of IL-17A and other inflammatory markers during the development of soybean meal-induced enteropathy in the distal intestine of Atlantic salmon (Salmo salar L.). , 2012, Cytokine.

[41]  Takeshi Yamamoto,et al.  Influence of dietary soy protein and peptide products on bile acid status and distal intestinal morphology of rainbow trout Oncorhynchus mykiss , 2012, Fisheries Science.

[42]  M. Øverland,et al.  Prevention of soya-induced enteritis in Atlantic salmon (Salmo salar) by bacteria grown on natural gas is dose dependent and related to epithelial MHC II reactivity and CD8α+ intraepithelial lymphocytes , 2012, British Journal of Nutrition.

[43]  L. Mydland,et al.  Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar) , 2012, BMC Veterinary Research.

[44]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[45]  M. Izquierdo,et al.  Improved feed utilization, intestinal mucus production and immune parameters in sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS) , 2011 .

[46]  Å. Krogdahl,et al.  High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.) , 2011 .

[47]  D. Gatlin,et al.  Effects of dietary prebiotics on growth performance, immune response and intestinal morphology of red drum (Sciaenops ocellatus) , 2010 .

[48]  Å. Krogdahl,et al.  Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids , 2010 .

[49]  V. Beneš,et al.  The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. , 2009, Clinical chemistry.

[50]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[51]  K. Sundell,et al.  Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.) , 2008, British Journal of Nutrition.

[52]  S. Denev,et al.  Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss) , 2007, Aquaculture International.

[53]  P. Klesius,et al.  Immune Response and Resistance to Stress and Edwardsiella ictaluri Challenge in Channel Catfish, Ictalurus punctatus, Fed Diets Containing Commercial Whole‐Cell Yeast or Yeast Subcomponents , 2007 .

[54]  Å. Krogdahl,et al.  Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.) , 2003 .

[55]  Zuzana Dobbie,et al.  Processing of gene expression data generated by quantitative real-time RT-PCR. , 2002, BioTechniques.

[56]  Å. Krogdahl,et al.  Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish , 1996 .

[57]  Å. Krogdahl,et al.  Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar) : a morphological study , 1991 .

[58]  M. W. Kearsley,et al.  Saponin content of soya and some commercial soya products by means of high‐performance liquid chromatography of the sapogenins , 1986 .

[59]  I. Liener,et al.  Contribution of trypsin inhibitors to the deleterious effects of unheated soybeans fed to rats. , 1973, The Journal of nutrition.

[60]  C. Ray,et al.  Analysis of the Gut Microbiome of Nile Tilapia Oreochromis Niloticus L. Fed Diets Supplemented with Previda® and Saponin , 2017 .

[61]  Enrique Blanco Gonzalez,et al.  The development of the Norwegian wrasse fishery and the use of wrasses as cleaner fish in the salmon aquaculture industry , 2017 .

[62]  R. Reda,et al.  Beta-Glucans and Mannan Oligosaccharides Enhance Growth and Immunity in Nile Tilapia , 2015 .