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Functional Diets Modulate lncRNA-Coding RNAs and Gene Interactions in the Intestine of Rainbow Trout Oncorhynchus mykiss

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Abstract

The advent of functional genomics has sparked the interest in inferring the function of non-coding regions from the transcriptome in non-model species. However, numerous biological processes remain understudied from this perspective, including intestinal immunity in farmed fish. The aim of this study was to infer long non-coding RNA (lncRNAs) expression profiles in rainbow trout (Oncorhynchus mykiss) fed for 30 days with functional diets based on pre- and probiotics. For this, whole transcriptome sequencing was conducted through Illumina technology, and lncRNAs were mined to evaluate transcriptional activity in conjunction with known protein sequences. To detect differentially expressed transcripts, 880 novels and 9067 previously described O. mykiss lncRNAs were used. Expression levels and genome co-localization correlations with coding genes were also analyzed. Significant differences in gene expression were primarily found in the probiotic diet, which had a twofold downregulation of lncRNAs compared to other treatments. Notable differences by diet were also evidenced between the coding genes of distinct metabolic processes. In contrast, genome co-localization of lncRNAs with coding genes was similar for all diets. This study contributes novel knowledge regarding lncRNAs in fish, suggesting key roles in salmons fed with in-feed additives with the capacity to modulate the intestinal homeostasis and host health.

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References

  • Al-Tobasei R, Paneru B, Salem M (2016) Genome-wide discovery of long non-coding RNAs in rainbow trout. PLoS One 11:e0148940

    Article  PubMed  PubMed Central  Google Scholar 

  • Bao M-H et al (2016) Impact of high fat diet on long non-coding RNAs and messenger RNAs expression in the aortas of ApoE (−/−) mice. Sci Rep 6:34161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batista PJ, Chang HY (2013) Long noncoding RNAs: cellular address codes in development and disease. Cell 152:1298–1307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boltana S, Valenzuela-Miranda D, Aguilar A, Mackenzie S, Gallardo-Escarate C (2016) Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during ISAV-infected Atlantic salmon (Salmo salar). Sci Rep 6:22698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boltaña S, Valenzuela-Miranda D, Aguilar A, Mackenzie S, Gallardo-Escárate C (2016) Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during ISAV-infected Atlantic salmon (Salmo salar). Sci Rep 6:22698

    Article  PubMed  PubMed Central  Google Scholar 

  • Dimitroglou A, Merrifield DL, Spring P, Sweetman J, Moate R, Davies SJ (2010) Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture 300:182–188

    Article  CAS  Google Scholar 

  • Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Wilson A (2009) Geneious v4. 8. http://www.geneious.com

  • Gatesoupe F-J et al (2014) The effects of dietary carbohydrate sources and forms on metabolic response and intestinal microbiota in sea bass juveniles, Dicentrarchus labrax. Aquaculture 422–423:47–53

    Article  Google Scholar 

  • Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154

    Article  PubMed  Google Scholar 

  • Goodier JL, Davidson WS (1994) Tc1 transposon-like sequences are widely distributed in salmonids. J Mol Biol 241:26–34

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Fu X, Li N, Lin Q, Liu L, Wu S (2016) Molecular characterization and expression pattern of tumor suppressor protein p53 in mandarin fish, Siniperca chuatsi following virus challenge. Fish Shellfish Immunol 51:392–400

    Article  CAS  PubMed  Google Scholar 

  • Hai NV (2015) The use of probiotics in aquaculture. J Appl Microbiol 119:917–935

    Article  CAS  PubMed  Google Scholar 

  • Hoseinifar SH, Ringø E, Shenavar Masouleh A, Esteban MÁ (2016) Probiotic, prebiotic and synbiotic supplements in sturgeon aquaculture: a review. Rev Aquac 8:89–102

    Article  Google Scholar 

  • Jiang L, Liu W, Zhu A, Zhang J, Zhou J, Wu C (2016) Transcriptome analysis demonstrate widespread differential expression of long noncoding RNAs involve in Larimichthys crocea immune response. Fish Shellfish Immunol 51:1–8

    Article  CAS  PubMed  Google Scholar 

  • Kamada N, Nunez G (2014) Regulation of the immune system by the resident intestinal bacteria. Gastroenterology 146:1477–1488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelder T, Stroeve JHM, Bijlsma S, Radonjic M, Roeselers G (2014) Correlation network analysis reveals relationships between diet-induced changes in human gut microbiota and metabolic health. Nutr Diabetes 4:e122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornfeld JW, Bruning JC (2014) Regulation of metabolism by long, non-coding RNAs. Front Genet 5:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Krakowsky RH, Tollefsbol TO (2015) Impact of nutrition on non-coding RNA epigenetics in breast and gynecological cancer. Front Nutr 2:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Krasnov A, Koskinen H, Afanasyev S, Mölsä H (2005) Transcribed Tc1-like transposons in salmonid fish. BMC Genomics 6:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Lara-Flores M, Olvera-Novoa MA, Guzmán-Méndez BZE, López-Madrid W (2003) Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216:193–201

    Article  Google Scholar 

  • Li S, Chen X, Hao G, Geng X, Zhan W, Sun J (2016) Identification and characterization of a novel NOD-like receptor family CARD domain containing 3 gene in response to extracellular ATP stimulation and its role in regulating LPS-induced innate immune response in Japanese flounder (Paralichthys olivaceus) head kidney macrophages. Fish Shellfish Immunol 50:79–90

    Article  CAS  PubMed  Google Scholar 

  • Liang LX, Ai LY, Qian J, Fang JY, Xu J (2015) Long noncoding RNA expression profiles in gut tissues constitute molecular signatures that reflect the types of microbes. Sci Rep 5:11763

    Article  PubMed  PubMed Central  Google Scholar 

  • Mansfield GS, Desai AR, Nilson SA, Van Kessel AG, Drew MD, Hill JE (2010) Characterization of rainbow trout (Oncorhynchus mykiss) intestinal microbiota and inflammatory marker gene expression in a recirculating aquaculture system. Aquaculture 307:95–104

    Article  CAS  Google Scholar 

  • Maricchiolo G et al (2015) Saccharomyces cerevisiae var. boulardii preserves the integrity of intestinal mucosa in gilthead seabream, Sparus aurata subjected to a bacterial challenge with Vibrio anguillarum. Aquac Res 48(2):725–728

    Article  Google Scholar 

  • Martin SAM, Dehler CE, Król E (2016) Transcriptomic responses in the fish intestine. Dev Comp Immunol 64:103–117

    Article  CAS  PubMed  Google Scholar 

  • Mattick JS, Rinn JL (2015) Discovery and annotation of long noncoding RNAs. Nat Struct Mol Biol 22:5–7

    Article  CAS  PubMed  Google Scholar 

  • Nam B-H, Kim Y-O, Kong HJ, Kim W-J, Lee S-J, Choi T-J (2009) Identification and characterization of the prepro-vasoactive intestinal peptide gene from the teleost Paralichthys olivaceus. Vet Immunol Immunopathol 127:249–258

    Article  CAS  PubMed  Google Scholar 

  • Nunez-Acuna G, Goncalves AT, Valenzuela-Munoz V, Pino-Marambio J, Wadsworth S, Gallardo-Escarate C (2015) Transcriptome immunomodulation of in-feed additives in Atlantic salmon Salmo salar infested with sea lice Caligus rogercresseyi. Fish Shellfish Immunol 47:450–460

    Article  CAS  PubMed  Google Scholar 

  • Ortuño J, Cuesta A, Rodríguez A, Esteban MA, Meseguer J (2002) Oral administration of yeast, Saccharomyces cerevisiae, enhances the cellular innate immune response of gilthead seabream (Sparus aurata L.) Vet Immunol Immunopathol 85:41–50

    Article  PubMed  Google Scholar 

  • Paneru B, Al-Tobasei R, Palti Y, Wiens GD, Salem M (2016) Differential expression of long non-coding RNAs in three genetic lines of rainbow trout in response to infection with Flavobacterium psychrophilum. Sci Rep 6:36032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Sanchez J, Estensoro I, Redondo MJ, Calduch-Giner JA, Kaushik S, Sitja-Bobadilla A (2013) Mucins as diagnostic and prognostic biomarkers in a fish-parasite model: transcriptional and functional analysis. PLoS One 8:e65457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radice AD, Bugaj B, Fitch DHA, Emmons SW (1994) Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish. Mol Gen Genet 244:606–612

    Article  CAS  PubMed  Google Scholar 

  • Reed KM (1999) Tc1-like transposable elements in the genome of lake trout (Salvelinus namaycush). Mar Biotechnol 1:60–67

    Article  CAS  PubMed  Google Scholar 

  • Ringø E et al (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr 22:219–282

    Article  Google Scholar 

  • Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166

    Article  CAS  PubMed  Google Scholar 

  • Ross SA, Davis CD (2014) The emerging role of microRNAs and nutrition in modulating health and disease. Annu Rev Nutr 34:305–336

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

  • Ruiz-Orera J et al (2014) Long non-coding RNAs as a source of new peptides. elife 3:e03523

    Article  PubMed  PubMed Central  Google Scholar 

  • Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, Rawls JF (2012) Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12:277–288

    Article  CAS  PubMed  Google Scholar 

  • Torrecillas S, Makol A, Betancor MB, Montero D, Caballero MJ, Sweetman J, Izquierdo M (2013) Enhanced intestinal epithelial barrier health status on European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 34:1485–1495

    Article  CAS  PubMed  Google Scholar 

  • Torrecillas S, Montero D, Caballero MJ, Robaina L, Zamorano MJ, Sweetman J, Izquierdo M (2015) Effects of dietary concentrated mannan oligosaccharides supplementation on growth, gut mucosal immune system and liver lipid metabolism of European sea bass (Dicentrarchus labrax) juveniles. Fish Shellfish Immunol 42:508–516

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Fu L, Koganti PP, Wang L, Hand JM, Ma H, Yao J (2016) Identification and functional prediction of large intergenic noncoding RNAs (lincRNAs) in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol (NY) 18:271–282

    Article  CAS  Google Scholar 

  • Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293–5300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J et al (2016) Characterization of long non-coding RNA transcriptome in high-energy diet induced nonalcoholic steatohepatitis minipigs. Sci Rep 6:30709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao L et al (2016) Long noncoding RNA SPRY4-IT1 regulates intestinal epithelial barrier function by modulating the expression levels of tight junction proteins. Mol Biol Cell 27:617–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young RS, Ponting CP (2013) Identification and function of long non-coding RNAs. Essays Biochem 54:113–126

    Article  CAS  PubMed  Google Scholar 

  • Zorriehzahra MJ, Delshad ST, Adel M, Tiwari R, Karthik K, Dhama K, Lazado CC (2016) Probiotics as beneficial microbes in aquaculture: an update on their multiple modes of action: a review. Vet Q 36(4):228–241

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was financially supported by CONICYT-Chile through the grants FONDECYT Postdoctoral 3140183 and FONDAP-INCAR 15110027. The authors thank EWOS-Cargill for supplying the feed and oil mixture for the trial and for granting access to experimental feeding unit in Coronel Chile. The authors would also like to thank Fernando Vidal and Alejandro Capdeville for the technical support during experimental feed preparation.

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Authors and Affiliations

  1. Interdisciplinary Center for Aquaculture Research (INCAR), Department of Oceanography, University of Concepción, Concepción, Chile

    Gustavo Núñez-Acuña, Camille Détrée, Cristian Gallardo-Escárate & Ana Teresa Gonçalves

  2. Laboratory of Biotechnology and Aquatic Genomics, Interdisciplinary Center for Aquaculture Research (INCAR), University of Concepción, P.O. Box 160-C, Concepción, Chile

    Ana Teresa Gonçalves

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  1. Gustavo Núñez-Acuña
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  2. Camille Détrée
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  3. Cristian Gallardo-Escárate
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  4. Ana Teresa Gonçalves
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Corresponding author

Correspondence to Ana Teresa Gonçalves.

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Ethical Statement

All animals used in this study were treated in accordance to the Biosecurity Regulations and Ethical Protocols approved by Universidad de Concepción Ethics Committee as a mandatory part of the Postdoctoral FONDECYT Grant 3140183 granted by the CONICYT-Chile.

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The authors declare that they have no conflicts of interest.

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Núñez-Acuña, G., Détrée, C., Gallardo-Escárate, C. et al. Functional Diets Modulate lncRNA-Coding RNAs and Gene Interactions in the Intestine of Rainbow Trout Oncorhynchus mykiss . Mar Biotechnol 19, 287–300 (2017). https://doi.org/10.1007/s10126-017-9750-z

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  • DOI: https://doi.org/10.1007/s10126-017-9750-z

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