Effects of Lactogen 13, a New Probiotic Preparation, on Gut Microbiota and Endocrine Signals Controlling Growth and Appetite of Oreochromis niloticus Juveniles
In the present study, Nile tilapia Oreochromis niloticus was used as experimental model to study the molecular effects of a new probiotic preparation, Lactogen 13 (Lactobacillus rhamnosus IMC 501® encapsulated with vegetable fat matrices by spray chilling and further indicated as probiotic microgranules), on growth and appetite during larval development. Probiotic microgranules were administered for 30 days to tilapia larvae starting from first feeding. Molecular analysis using high-throughput sequencing revealed that the probiotic could populate the gastrointestinal tract and modulate the microbial communities by significantly increasing the proportion of Lactobacillus as well as reducing the proportion of potential pathogens such as members of the Family Microbacteriaceae, Legionellaceae, and Weeksellaceae. Morphometric analysis evidenced that body weight and total length significantly increased after probiotic treatment. This increase coincided with the modulation of genes belonging to the insulin-like growth factors (igfs) system and genes involved on myogenesis, such as myogenin, and myogenic differentiation (myod). Alongside the improvement of growth, an increase of feed intake was evidenced at 40 days post-fertilization (dpf) in treated larvae. Gene codifying for signals belonging to the most prominent systems involved in appetite regulation, such as neuropeptide y (npy), agouti-related protein (agrp), leptin, and ghrelin were significantly modulated. These results support the hypothesis that gastrointestinal (GI) microbiota changes due to probiotic administration modulate growth and appetite control, activating the endocrine system of tilapia larvae.
KeywordsProbiotic Microbiome IGF Leptin Ghrelin
The authors thank Prof. A. Cresci (Synbiotec Srl, Camerino, Italy) and Dr. L. Bortolotto (Sintal Srl, Isola Vicentina Italy), who kindly provided expertise, probiotic strain, and facilities to produce the prototype of Lactogen 13. This study was supported by Mi.S.E. N. 2201 to Oliana Carnevali.
Compliance with Ethical Standards
Conflict of Interest
All authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
- 1.Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD et al (2017) Expert consensus document: the international scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Review of Gastroenterology and Hepatology 14:491–502Google Scholar
- 9.Addo S, Carrias AA, Williams MA, Liles MR, Terhune JS, Davis DA (2017) Effects of Bacillus subtilis strains and the prebiotic Previda on growth, immune parameters and susceptibility to Aeromonas hydrophila infection in Nile tilapia, Oreochromis niloticus. Aquac. Res. 48:4798–4810CrossRefGoogle Scholar
- 20.Geurden I, Mennigen J, Plagnes-Juan E, Veron V, Cerezo T, Mazurais D, Zambonino-Infante J, Gatesoupe J, Skiba-Cassy S, Panserat S (2014) High or low dietary carbohydrate: protein ratios during first-feeding affect glucose metabolism and intestinal microbiota in juvenile rainbow trout. J. Exp. Biol. 217:3396–3406CrossRefPubMedGoogle Scholar
- 21.Rocha F, Dias J, Geurden I, Dinis MT, Panserat S, Engrola S (2016) Dietary glucose stimulus at larval stage modifies the carbohydrate metabolic pathway in gilthead seabream (Sparus aurata) juveniles: an in vivo approach using C-14-starch. Comp Biochem Physiol A Mol Integr Physiol 201:189–199CrossRefPubMedGoogle Scholar
- 22.Avella MA, Olivotto I, Silvi S, Place AR, Carnevali O (2010) Effect of dietary probiotics on clownfish: a molecular approach to define how lactic acid bacteria modulate development in a marine fish. Am J Physiol-Reg I 298:R359–R371Google Scholar
- 26.Cecchini C, Verdenelli MC, Palmieri GF, Silvi S (2010) Evaluation of microgranulation of Lactobacillus rhamnosus IMC 501® and Lactobacillus paracasei IMC 502® with vegetable fats as an approach to prolonging viability during storage. J. Biotechnol. 21:28–31Google Scholar
- 27.Ogbonna CC, Cecchini C, Silvi S, Verdenelli MC, Coman MM, Orpianesi C, Cresci A (2011) Enhancing Italian traditional foods through the enrichment of functional ingredients. Agro Food Industry Hi-Tech 22:34–37Google Scholar
- 28.Han B, Long W, He J, Liu Y, Si Y, Tian L (2015) Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46:225e231CrossRefGoogle Scholar
- 30.Falcinelli S, Picchietti S, Rodiles A, Cossignani L, Merrifield DL, Taddei AR, Maradonna F, Olivotto I, Gioacchini G, Carnevali O (2015) Lactobacillus rhamnosus lowers zebrafish lipid content by changing gut microbiota and host transcription of genes involved in lipid metabolism. Sci. Rep. 5:9336CrossRefPubMedPubMedCentralGoogle Scholar
- 31.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010a) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
- 38.Andersen CL, Jensen JL, Ørntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245–5250CrossRefPubMedGoogle Scholar
- 43.Boguszewski CL, van der Lely AJ (2015) The role of the gastrointestinal tract in the control of energy balance. Transl Gastrointest Cancer 4:3–13Google Scholar
- 62.Besseau L, Fuentes M, Sauzet S, Beauchaud M, Chatain B, Coves D, Boeuf G, Falcón J (2013) Somatotropic axis genes are expressed before pituitary onset during zebrafish and sea bass development. Gen. Comp. Endocrinol. 94:141Google Scholar