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PLOS ONE  2013 

Candida utilis and Chlorella vulgaris Counteract Intestinal Inflammation in Atlantic Salmon (Salmo salar L.)

DOI: 10.1371/journal.pone.0083213

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Abstract:

Intestinal inflammation, caused by impaired intestinal homeostasis, is a serious condition in both animals and humans. The use of conventional extracted soybean meal (SBM) in diets for Atlantic salmon and several other fish species is known to induce enteropathy in the distal intestine, a condition often referred to as SBM induced enteropathy (SBMIE). In the present study, we investigated the potential of different microbial ingredients to alleviate SBMIE in Atlantic salmon, as a model of feed-induced inflammation. The dietary treatments consisted of a negative control based on fish meal (FM), a positive control based on 20% SBM, and four experimental diets combining 20% SBM with either one of the three yeasts Candida utilis (CU), Kluyveromyces marxianus (KM), Saccharomyces cerevisiae (SC) or the microalgae Chlorella vulgaris (CV). Histopathological examination of the distal intestine showed that all fish fed the SC or SBM diets developed characteristic signs of SBMIE, while those fed the FM, CV or CU diets showed a healthy intestine. Fish fed the KM diet showed intermediate signs of SBMIE. Corroborating results were obtained when measuring the relative length of PCNA positive cells in the crypts of the distal intestine. Gene set enrichment analysis revealed decreased expression of amino acid, fat and drug metabolism pathways as well as increased expression of the pathways for NOD-like receptor signalling and chemokine signalling in both the SC and SBM groups while CV and CU were similar to FM and KM was intermediate. Gene expression of antimicrobial peptides was reduced in the groups showing SBMIE. The characterisation of microbial communities using PCR-DGGE showed a relative increased abundance of Firmicutes bacteria in fish fed the SC or SBM diets. Overall, our results show that both CU and CV were highly effective to counteract SBMIE, while KM had less effect and SC had no functional effects.

References

[1]  Krogdahl ?, Penn M, Thorsen J, Refstie S, Bakke AM (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquacult Res 41: 333–344.
[2]  Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, et al. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38: 551–579.
[3]  van den Ingh TSGAM, Krogdahl ?, Olli JJ, Hendriks HGCJM, Koninkx JGJF (1991) Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar): a morphological study. Aquaculture 94: 297–305.
[4]  Penn MH, Bendiksen E?, Campbell P, Krogdahl ? (2011) High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture 310: 267–273.
[5]  Burrells C, Williams PD, Southgate PJ, Crampton VO (1999) Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet Immunol Immunopathol 72: 277–88.
[6]  Uran P, Goncalves A, Tavernethiele J, Schrama J, Verreth J, et al. (2008) Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 25: 751–760.
[7]  Krogdahl ?, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9: 361–71.
[8]  Baeverfjordl G, Krogdah ? (1996) Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 19: 375–387.
[9]  Marjara IS, Chikwati EM, Valen EC, Krogdahl ?, Bakke AM (2012) 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.). Cytokine 60: 186–96.
[10]  Kortner TM, Skugor S, Penn MH, Mydland LT, Djordjevic B, et al. (2012) Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar). BMC Vet Res 8: 101.
[11]  Bakke-McKellep AM, Fr?ystad MK, Lilleeng E, Dapra F, Refstie S, et al. (2007) Response to soy: T-cell-like reactivity in the intestine of Atlantic salmon, Salmo salar L. J Fish Dis. 30: 13–25.
[12]  Mansfield GS, Desai AR, Nilson SA, Kessel AGV, Drew MD, et al. (2010) Characterization of rainbow trout (Oncorhynchus mykiss) intestinal microbiota and inflammatory marker gene expression in a recirculating aquaculture system. Aquaculture 307: 95–104.
[13]  van den Ingh TSGAM, Olli JJ, Krogdahl ? (1996) Alcohol-soluble components in soybeans cause morphological changes in the distal intestine of Atlantic salmon, Salmo salar L. J Fish Dis. 19: 47–53.
[14]  Escaffre AM, Kaushik S, Mambrini M (2007) Morphometric evaluation of changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) due to fish meal replacement with soy protein concentrate. Aquaculture 273: 127–138.
[15]  Heyman M, Abed J, Lebreton C, Cerf-Bensussan N (2012) Intestinal permeability in coeliac disease: insight into mechanisms and relevance to pathogenesis. Gut 61: 1355–1364.
[16]  Khor B, Gardet A, Xavier RJ (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474: 307–17.
[17]  Romarheim OH, ?verland M, Mydland LT, Skrede A, Landsverk T (2011) Bacteria grown on natural gas prevent soybean meal-induced enteritis in Atlantic salmon. J Nutr 141: 124–30.
[18]  Romarheim OH, Hetland DL, Skrede A, Overland M, Mydland LT, et al.. (2012) 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 CD8 α+ intraepithelial lymphocytes. Br J Nutr: 1–9.
[19]  Romarheim OH, Landsverk T, Mydland LT, Skrede A, ?verland M (2013) Cell wall fractions from Methylococcus capsulatus prevent soybean meal-induced enteritis in Atlantic salmon (Salmo salar). Aquaculture 402–403: 13–18.
[20]  ?verland M, Karlsson A, Mydland LT, Romarheim OH, Skrede A (2013) Evaluation of Candida utilis, Kluyveromyces marxianus and Saccharomyces cerevisiae yeasts as protein sources in diets for Atlantic salmon (Salmo salar). Aquaculture 402–403: 1–7.
[21]  Janczyk P, Franke H, Souffrant W (2007) Nutritional value of Chlorella vulgaris: Effects of ultrasonication and electroporation on digestibility in rats. Anim Feed Sci Tech 132: 163–169.
[22]  Samarakoon K, Jeon YJ (2012) Bio-functionalities of proteins derived from marine algae – A review. Food Res Int 48: 948–960.
[23]  Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, et al. (1999) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 27: 29–34.
[24]  Manocha M, Khan WI (2012) Serotonin and GI Disorders: An Update on Clinical and Experimental Studies. Clin Trans Gastroenterol 3: e13.
[25]  Hashimoto T, Perlot T, Rehman A, Trichereau J, Ishiguro H, et al. (2012) ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 487: 477–481.
[26]  Samiec PS, Dahm LJ, Jones DP (2000) Glutathione S-transferase in mucus of rat small intestine. Toxicol Sci 54: 52–9.
[27]  Hylemon PB, Zhou H, Pandak WM, Ren S, Gil G, et al. (2009) Bile acids as regulatory molecules. J Lipid Res 50: 1509–1520.
[28]  Berge KE, Tian H, Graf GA, Yu L, Grishin NV, et al. (2000) Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science (80?) 290: 1771–5.
[29]  Kortner TM, Gu J, Krogdahl A, Bakke AM (2012) Transcriptional regulation of cholesterol and bile acid metabolism after dietary soyabean meal treatment in Atlantic salmon (Salmo salar L.). Br J Nutr: 1–12.
[30]  Hardin JA, Wallace LE, Wong JFK, O'loughlin EV, Urbanski SJ, et al. (2004) Aquaporin expression is downregulated in a murine model of colitis and in patients with ulcerative colitis, Crohn's disease and infectious colitis. Cell Tissue Res 318: 313–323.
[31]  Wells JM, Rossi O, Meijerink M, van Baarlen P (2011) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA 108 Suppl 14607–14.
[32]  Williams IR (2004) Chemokine receptors and leukocyte trafficking in the mucosal immune system. Immunol Res 29: 283–92.
[33]  Lomax AE, Fernandez E, Sharkey KA (2005) Plasticity of the enteric nervous system during intestinal inflammation. Neurogastroenterol Motil 17: 4–15.
[34]  Frankel G, Phillips AD, Rosenshine I, Dougan G, Kaper JB, et al. (1998) Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30: 911–21.
[35]  Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7: 349–359.
[36]  Kimball SR, Jefferson LS (2006) New functions for amino acids: effects on gene transcription and translation. Am J Clin Nutr 83: 500S–507S.
[37]  Findley MK, Koval M (2009) Regulation and roles for claudin-family tight junction proteins. IUBMB Life 61: 431–7.
[38]  Muise AM, Walters TD, Glowacka WK, Griffiths AM, Ngan BY, et al. (2009) Polymorphisms in E-cadherin (CDH1) result in a mis-localised cytoplasmic protein that is associated with Crohn's disease. Gut 58: 1121–1127.
[39]  Bevins CL, Salzman NH (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Micro 9: 356–68.
[40]  Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, et al. (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94: 5967–72.
[41]  Refstie S, Bakke-Mckellep AM, Penn MH, Sundby A, Shearer KD, et al. (2006) Capacity for digestive hydrolysis and amino acid absorption in Atlantic salmon (Salmo salar) fed diets with soybean meal or inulin with or without addition of antibiotics. Aquaculture 261: 392–406.
[42]  Nordrum S, Bakke-McKellep AM, Krogdahl A, Buddington RK (2000) Effects of soybean meal and salinity on intestinal transport of nutrients in Atlantic salmon (Salmo salar L.) and rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B, Biochem Mol Biol 125: 317–35.
[43]  Sahlmann C, Sutherland BJG, Kortner TM, Koop BF, Krogdahl ?, et al. (2013) Early response of gene expression in the distal intestine of Atlantic salmon (Salmo salar L.) during the development of soybean meal induced enteritis. Fish Shellfish Immunol 34: 599–609.
[44]  Artis D (2008) Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8: 411–20.
[45]  Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, et al. (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science (80- ) 307: 731–4.
[46]  Nuding S, Fellermann K, Wehkamp J, Stange EF (2007) Reduced mucosal antimicrobial activity in Crohn's disease of the colon. Gut 56: 1240–1247.
[47]  Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, et al. (2005) Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci USA 102: 18129–34.
[48]  Sveinbj?rnsson B, Olsen R, Paulsen S (1996) Immunocytochemical localization of lysozyme in intestinal eosinophilic granule cells (EGCs) of Atlantic salmon, Salmo salar L. J Fish Dis. 19: 349–355.
[49]  Silphaduang U, Colorni A, Noga EJ (2006) Evidence for widespread distribution of piscidin antimicrobial peptides in teleost fish. Dis Aquat Org 72: 241–52.
[50]  Desai AR, Links MG, Collins SA, Mansfield GS, Drew MD, et al. (2012) Effects of plant-based diets on the distal gut microbiome of rainbow trout (Oncorhynchus mykiss). Aquaculture 350–353: 134–142.
[51]  Bakke-Mckellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, et al. (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97: 699–713.
[52]  Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sj?berg J, et al. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76–82.
[53]  Kleiveland CR, Hult LTO, Spetalen S, Kaldhusdal M, Christofferesen TE, et al. (2013) The noncommensal bacterium Methylococcus capsulatus (Bath) ameliorates dextran sulfate (Sodium Salt)-Induced Ulcerative Colitis by influencing mechanisms essential for maintenance of the colonic barrier function. Appl Environ Microbiol 79: 48–56.
[54]  ?verland M, S?rensen M, Storebakken T, Penn M, Krogdahl ?, et al. (2009) Pea protein concentrate substituting fish meal or soybean meal in diets for Atlantic salmon (Salmo salar)– Effect on growth performance, nutrient digestibility, carcass composition, gut health, and physical feed quality. Aquaculture 288: 305–311.
[55]  ?verland M, Tauson AH, Shearer K, Skrede A (2010) Evaluation of methane-utilising bacteria products as feed ingredients for monogastric animals. Arch Anim Nutr 64: 171–89.
[56]  Gentleman RC, Carey VJ, Bates DM (2004) others (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5: R80.
[57]  Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors, Bioinformatics and Computational Biology Solutions Using R and Bioconductor, New York: Springer. 397–420.
[58]  Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–93.
[59]  Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, et al. (2001) Missing value estimation methods for DNA microarrays. Bioinformatics 17: 520–5.
[60]  Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
[61]  Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182–5.
[62]  H?nzelmann S, Castelo R, Guinney J (2013) GSVA: gene set variation analysis for microarray and RNA-Seq data. BMC Bioinformatics 14: 7.
[63]  Benjamini Y, Yosef H (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289–300.
[64]  Vandesompele J, Preter KD, Pattyn F, Poppe B, Roy NV, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
[65]  Yu Z, Morrison M (2004) Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Appl Environ Microbiol 70: 4800–6.
[66]  Zar JH (1996) Biostatistical Analysis, Prentice Hall, chapter Multiple Comparisons. 3rd edition, 211–33.
[67]  Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36–42.

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