Combined Effects of Dietary Bacillus subtilis and Trans-cinnamic Acid on Growth Performance, Whole Body Compositions, Digestive Enzymes and Intestinal bacteria in Rainbow Trout (Oncorhynchus mykiss)

Authors

  • Sevdan YILMAZ Department of Aquaculture, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey
  • Nergiz ÇOBAN Department of Aquaculture, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey
  • Sebahattin ERGÜN Department of Aquaculture, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey
  • Murat YIGIT Department of Marine Technology, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey
  • Ekrem Şanver ÇELIK Department of Marine Science, Faculty of Marine Sciences and Technology, Çanakkale Onsekiz Mart University, Çanakkale, Turkey

DOI:

https://doi.org/10.30564/jzr.v1i2.1682

Abstract

In this study, the combined effects of dietary Bacillus subtilis (BS, 10 7 g/cfu) and different levels (0.025%, 0.050%, 0.075% and 0.150%) of trans-cinnamic acid (CA) on fish growth performance, whole body compositions, digestive enzymes, intestinal bacteria and internal organ index of rainbow trout (Oncorhynchus mykiss) were investigated. Six different experimental groups including control group (C), C+BS, 0.025%CA+BS, 0.050%CA+BS, 0.075CA+BS, 0.150%CA+BS) were established. According to the results obtained, growth performance, whole body compositions and digestive pH were not statistically significant among groups. Further, no significant differences were found between experimental groups in terms of the intestinal enzymes (trypsin, alkaline phosphatase and lipase) and gastric pepsin. Significantly higher levels of intestinal amylase were found in the control+BS, 0.025%CA+BS, 0.050% CA+BS, and 0.075%CA+BS compared to the control and 0.150%CA+BS groups. Moreover, coliform and Enterobacteriaceae counts were highest in the control+B. subtilis and lowest in the 0.150% CA + B. subtilis groups.

Keywords:

B. subtilis, cinnamic acid, organic acid, probiotic, Oncorhynchus mykiss

References

[1] Park, Y., Lee, S., Hong, J., Kim, D., Moniruzzaman, M. and Bai, S.C. (2016), Use of probiotics to enhance growth, stimulate immunity and confer disease resistance to Aeromonas salmonicida in rainbow trout (Oncorhynchus mykiss), Aquaculture Research, 1–11.

[2] Yılmaz, S. and Ergün, S. (2018), Trans-cinnamic acid application for rainbow trout (Oncorhynchus mykiss): I. Effects on haematological, serum biochemical, non-specific immune and head kidney gene expression responses, Fish and Shellfish Immunology, 78, 140–157.

[3] Chi, C., Giri, S.S., Jun, J.W., Yun, S., Kim, H.J., Kim, S.G. and Park, S.C. (2016), Immune response of the bay scallop, Argopecten irradians, after exposure to the algicide palmitoleic acid, Fish Shellfish Immunol., 57, 371–378.

[4] Nayak, S. (2010) Probiotics and immunity: a fish perspective, Fish Shellfish Immunol., 29 (1), 2–14.

[5] Bharathi, S., Antony, C., Cbt, R., Arumugam, U., Ahilan, B. and Aanand, S. (2019), Functional feed additives used in fish feeds, International Journal of Fisheries and Aquatic Studies, 7(3), 44-52.

[6] Hassaan, M., Soltan, M., Jarmołowicz, S. and Abdo, H. (2018), Combined effects of dietary malic acid and Bacillus subtilis on growth, gut microbiota and blood parameters of Nile tilapia (Oreochromis niloticus), Aquaculture Nutrition, 24, 83–93, https ://doi.org/10.1111/anu.12536.

[7] Kamgar, M. and Ghane M. (2012), Evalution of Bacillus subtilis effect as probiotic on hematological parameters of rainbow trout, Oncorhynchus mykiss (Walbaum) following experimental infection with Streptococcus iniae, Journal of fisheries and aquatic science, 7(6), 422-430.

[8] Vivas, J., Riano, J., Carracedo, B., Razquin, B. E., Lopez-Fierro, P., Naharro, G. and Villena, A. J. (2004), The auxotrophic aroA mutant of A. hydrophila as alive attenuated vaccine against A. salmonicida infections in rainbow trout, Fish & Shellfish Immunology, 16, 193-206.

[9] Bagheri, T., Hedayati, S. A., Yavari, V., Alizade, M. and Farzanfar, A. (2008), Growth, Survival and Gut Microbial Load of rainbow trout, Onchorhynchus mykiss (Walbaum) Fry Given Diet Supplemented with Probiotic during the Two Months of First Feeding, Journal of Fisheries and Aquatic Science, 8, 43-48.

[10] Hung, A. T. Y., Su, T. M., Liao, C. W. and Lu, J. J. (2008), Effect of Probiotic Combination Fermented Soybean Meal on Growth Performance, Lipid Metabolism and Immunological Response of Growing-Finishing Pigs, Asian Journal of Animal and Veterinary Advances, 3, 431-436.

[11] Zhou, Q., Li K., Jun, X. and Bo, L. (2009), Role and Functions of beneficial microorganisms in sustainable aquaculture, Bioresource Technology, 100,3780-3786.

[12] Son, V. M., Chang, C. C., Wu, M. C., Guu, Y. K., Chiu, C. H. and Cheng, W. (2009), Dietary administration of probiotic, Lactobacllus plantarum, enhanced the growth, innate immune responses and disease resistance of grouper Epinephelus coioides, Fish & Shellfish immunology, 26, 691-698.

[13] Agouz, H. M. and Anwer, W. (2011), Effect of Biogen® and Myco-Ad® on the Growth Performance of Common Carp (Cyprinus carpio) Fed a Mycotoxin Contaminated Aquafeed, Journal of Fisheries and Aquatic Science, 6 (3), 334–345.

[14] Zaineldin, A.I., Hegazi, S., Koshio, S., Ishikawa, M., Bakr, A., El-Keredy, A.M.S., Dawood, M.A.O., Dossou, S., Wang, W. and Yukun, Z. (2018), Bacillus subtilis as probiotic candidate for red sea bream: Growth performance, oxidative status, and immune response traits, Fish and Shellfish Immunology, 79, 303–312.

[15] Dawood, M.A., Koshio, S., Ishikawa, M., El-Sabagh, M., Esteban, M.A. and Zaineldin, A.I., (2016), Probiotics as an environment-friendly approach to enhance red sea bream, Pagrus major growth, immune response and oxidative status, Fish Shellfish Immunol., 57, 170–178.

[16] Adel, M., Yeganeh, S., Dawood, M.A.O., Safari, R. and Radhakrishnan, S. (2017), Effects of Pediococcus pentosaceus supplementation on growth performance, intestinal microflora and disease resistance of white shrimp, Litopenaeus vannamei, Aquacult. Nutr., 23(6), 1401–1409.

[17] Abdelkhalek, N.K., Eissa, I.A., Ahmed, E., Kilany, O.E., El-Adl, M., Dawood, M.A.O., Hassan, A.M., Abdel-Daim, M.M., (2017), Protective role of dietary Spirulina platensis against diazinon-induced Oxidative damage in Nile tilapia; Oreochromis niloticus, Environ. Toxicol. Pharmacol., 54, 99–104.

[18] Sahraei, F., Ahari, H. and Kakoolaki, S., (2019) Effect of Bacillus subtilis as a probiotic on protein, lipid content, and trypsin and chymotrypsin enzymes in rainbow trout biometry (Oncorhynchus mykiss), Aquaculture International, 27, 141–153.

[19] Mombelli B. and Gismondo M.R. (2000) The use of probiotics in medical practice, Int J Antimicrob Agents, 16, 531–536.

[20] Yılmaz, S., Ergün, S., Yiğit, M., Çelik, E.Ş. (2019a), Effect of combination of dietary Bacillus subtilis and trans‐cinnamic acid on innate immune responses and resistance of rainbow trout, Oncorhynchus mykiss to Yersinia ruckeri, Aquaculture Research., 2019,00:1–14.

[21] Yılmaz, S., 2017. The Effect of Dietary Cinnamic Acid or Bacillus subtilis on Growth Performance and Immunological Parameters in Rainbow Trout, Department of Aquaculture, Çanakkale Onsekiz Mart University, Graduate School of Natural and Applied Sciences, Türkiye, p. 210.

[22] Said, S., Neves, F.M. and Griffiths, A.J.F. (2004), Cinnamic acid inhibits the growth of the fungus Neurospora crassa, but is eliminated as acetophenone, Int. Biodeterior. Biodegrad, 54(1), 1–6.

[23] Sova, M. (2012), Antioxidant and antimicrobial activities of cinnamic acid derivatives, Mini Rev. Med. Chem., 12(8), 749–767.

[24] Pontiki, E., Hadjipavlou-Litina, D., Litinas, K., Geromichalos, G. (2014) Novel cinnamic acid derivatives as antioxidant and anticancer agents: design, synthesis and modeling studies, Molecules, 19(7), 9655–9674.

[25] Liu, L., Hudgins, W.R., Shack, S., Yin, M.Q. and Samid, D. (1995), Cinnamic acid - a natural product with potential use in cancer intervention, Int. J. Canc., 62(3), 345–350.

[26] Fernandez, M., Saenz, M. and Garcia, M. (1998), Natural Products: anti-inflammatory activity in rats and mice of phenolic acids isolated from Scrophularia frutescens, J. Pharm. Pharmacol., 50(10), 1183–1186.

[27] Prasad, V.G.N.V., Swamy, P.L., Rao, T.S. and Rao, G.S. (2014) Antibacterial synergy between quercetin and polyphenolic acids against bacterial pathogens of fish, Asian Pac. J. Trop. Dis., 4, S326–S329.

[28] Yılmaz, S. and Ergün S. (2013), Chickweed (Stellaria media) Leaf Meal as a Feed Ingredient for Tilapia (Oreochromis mossambicus), Journal of Applied Aquaculture, 25(4), 329-336.

[29] AOAC (1998), Official methods of analysis of AOAC International, AOAC Int., Gaithersburg, MD.

[30] Folch, J., Lees, M. and Sloane-Stanley, G. H. (1957), A simple method for the isolation and purification of total lipids from animal tissues, J biol chem, 226(1), 497-509.

[31] Anonymous (2005), Merck Gıda Mikrobiyolojisi Uygulamaları. Ed: A. K. Halkman, Başak Matbaacılık Ltd. Şti., Ankara.

[32] Merrifield, D. L., Dimitroglou, A., Bradley, G., Baker, R. T. M. and Davies, S. J. (2010), Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilization, intestinal bacteria and related health criteria, Aquaculture Nutrition, 16(5), 504-510.

[33] Giannenas, I., Triantafillou, E., Stavrakakis, S., Margaroni, M., Mavridis, S., Steiner, T. and Karagouni, E. (2012), Assessment of dietary supplementation with carvacrol or thymol containing feed additives on performance, intestinal bacteria and antioxidant status of rainbow trout (Oncorhynchus mykiss), Aquaculture, 350, 26-32.

[34] Šyvokienė, J. and Vosylienė, M.Z. (2013), Impact of copper and zinc mixture on bacterial flora of digestive tract of rainbow trout (Oncorhynchus mykiss), Journal of environmental engineering and landscape management, 21(4), 288–295.

[35] Bradford, M.M. (1976), A rapid and sensitive method for the quantization of protein utilizing the principle of dye- protein binding, Analytical Biochemistry, 72, 248-254.

[36] Faulk, C. K., Benninghoff, A. D. and Holt, G. J. (2007), Ontogeny of the gastrointestinal tract and selected digestive enzymes in cobia Rachycentron canadum (L.), Journal of Fish Biology, 70(2), 567-583.

[37] Jiang, H., and Wang, X. (2012), Time-dependent nanogel aggregation for naked-eye assays of α-amylase activity, Analyst, 137(11), 2582-2587.

[38] German, D. P., Horn, M. H. and Gawlicka, A. (2004), Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects, Physiological and Biochemical Zoology, 77(5), 789-804.

[39] Worthington, V. (1993), Worthington Enzyme Manual. Enzymes and Related Biochemicals Worthington Chemical, New Jersey, US. 399 pp.

[40] Katya, K., Park, G., Bharadwaj, A.S., Browdy, C.L., Vazquez-Anon, M. and Bai, S.C. (2018), Organic acids blend as dietary antibiotic replacer in marine fish olive flounder, Paralichthys olivaceus, Aquaculture Research, 49, 2861–2868.

[41] Lin Y. and Cheng M. (2017), Effects of dietary organic acid supplementation on the growth, nutrient digestibility and intestinal histology of the giant grouper Epinephelus lanceolatus fed a diet with soybean meal, Aquaculture, 469, 106–111.

[42] Nesara, K., Jayaraj, E., Amoga, K. and Sandeep, C. (2018). Effects of dietary probiotic and organic acid alone and in combination on the growth performance of Indian major carp, Labeo rohita, Journal of Experimental Zoology, 21, 805–812.

[43] Yılmaz, S., Ergun, S., Çelik, E. S., Yigit, M. and Bayizit, C. (2019b), Dietary trans-cinnamic acid application for rainbow trout (Oncorhynchus mykiss): II. Effect on antioxidant status, digestive enzyme, blood biochemistry and liver antioxidant gene expression responses, Aquaculture Nutrition, https ://doi.org/10.1111/anu.12935.

[44] Wu, Z. X., Feng, X., Xie, L. L., Peng, X. Y., Yuan, J. and Chen, X. X. (2012), Effect of probiotic Bacillus subtilis Ch9 for grass carp, Ctenopharyngodon idella (Valenciennes, 1844), on growth performance, digestive enzyme activities and intestinal microflora, Journal of Applied Ichthyology, 28(5), 721–727. https ://doi. org/10.1111/j.1439-0426.2012.01968.x.

[45] Hoa, N. T., Baccigalupi, L., Huxham, A., Smertenko, A., Van, P., Ammendola, S., Ricca, E. and Cutting, S. M. (2000), Characterization of bacillus species used for oral bacteriotherapy and bacterioprophylaxis of gastrointestinal disorders, Appl. Environ. Microbiol., 66, 5241–5247.

[46] McCarthy, J., OMahony, L., OCallaghan, L., Sheil, B., Vaughan, E. E., Fitzsimons, N., Fitzgibbon, J., OSullivan, G. C., Kiely, B., Collins, J. K. and Shanahan, F. (2003), Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance, Gut, 52, 975–980.

[47] Ng, W. K. and Koh, C. B. (2017), The utilization and mode of action of organic acids in the feeds of cultured aquatic animals, Reviews in Aquaculture, 9(4) 342–368. https://doi.org/10.1111/raq.12141.

[48] Yilmaz, S., Sova, M., and Ergün, S. (2018), Antimicrobial activity of trans cinnamic acid and commonly used antibiotics against important fish pathogens and non‐pathogenic isolates, Journal of Applied Microbiology, 125(6), 1714–1727. https ://doi.org/10.1111/jam.14097

[49] Ueberschar, B. (1995), The use of tryptic enzyme activity measurement as a nutritional condition index: laboratory calibration data and field application, ICES Mar. Sci. Symp., 201, 119–129.

[50] Suzer, C., Çoban, D., Okan, K. H., Saka, S., Firat, K., Otgucuoğlu, O. and Küçüksari, H. (2008), Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities, Aquaculture, 280, 140–145.

[51] Chen, Y. J., Luo, L., Zhang, G. Z., Li, Z., Bai, F. J., Shi, Y. Q., and Yang, H. S. (2016), Effect of dietary L‐malic acid supplementation on growth, feed utilization and digestive function of juvenile GIFT tilapia Oreochromis niloticus (Linnaeus, 1758), Journal of Applied Ichthyology, 32(6), 1118–1123. https://doi.org/10.1111/jai.13119.

[52] Oliveira, R.V., Oliveira, M.C. and Pelli, A., (2017), Disease Infection by Enterobacteriaceae Family in Fishes: A Review, J Microbiol Exp, 4(5), 00128.

[53] Al-Harbi, A.H. (2003), Faecal coliforms in pond water, sediments and hybrid tilapia Oreochromis niloticus ×Oreochromis aureus in Saudi Arabia, Aquaculture Research, 34, 517-524.

[54] Kaneko, S. (1971), Microbiological study of fresh fish, NewFood Industry, 13, 76-80.

[55] Geldreich, E.E. and Clarke, N.A. (1966), Bacterial pollution indicators in the intestinal tract of freshwater fish, Applied Microbiology, 14, 429-437.

[56] Cohen, J. and Shuval, H.I. (1973), Coliforms, fecal coliform and fecal streptococci as indicators of water pollution, Water Soil Pollution, 2, 85-95.

[57] Hadidi, S., Glenney, G. W., Welch, T. J., Silverstein, J. T. and Wiens, G. D. (2008), Spleen size predicts resistance of Rainbow Trout to Flavobacterium psychrophilum challenge. Journal of Immunology, 180, 4156–4165.

[58] Yılmaz, S., Ergün S. and Çelik, E.Ş. (2013), Effect of Dietary Herbal Supplements on Some Physiological Conditions of Sea Bass Dicentrarchus labrax, Journal of Aquatic Animal Health, 25, 98–103.

[59] Anderson, D. P. (1974), Fish immunology. T.F.H. Publications, Neptune City, New Jersey.

[60] Kumaran, S., Deivasigamani, B., Alagappan, K. M. and Sakthivel, M. (2010), Infection and immunization trials of Asian Seabass (Lates calcarifer) against fish pathogen Vibrio anguillarum, Journal of Environmental Biology, 31, 539–541.

[61] Wiens, G. D., and Vallejo R. L. (2010), Temporal and pathogen-load dependent changes in Rainbow Trout (Oncorhynchus mykiss) immune response traits following challenge with biotype 2 Yersinia ruckeri, Fish and Shellfish Immunology, 29, 639–647.

[62] Yilmaz, S., Ergün, S., & Yıgıt, M. (2018). Effects of dietary FARMARIN® XP supplement on immunological responses and disease resistance of rainbow trout (Oncorhynchus mykiss). Aquaculture, 496, 211-220.

Downloads

Issue

Vol. 1 , Iss. 2 (April 2019)

Article Type

Articles

License

Copyright and Licensing

The authors shall retain the copyright of their work but allow the Publisher to publish, copy, distribute, and convey the work.

Journal of Zoological Research publishes accepted manuscripts under Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0). Authors who submit their papers for publication by Journal of Zoological Research agree to have the CC BY-NC 4.0 license applied to their work, and that anyone is allowed to reuse the article or part of it free of charge for non-commercial use. As long as you follow the license terms and original source is properly cited, anyone may copy, redistribute the material in any medium or format, remix, transform, and build upon the material.

License Policy for Reuse of Third-Party Materials

If a manuscript submitted to the journal contains the materials which are held in copyright by a third-party, authors are responsible for obtaining permissions from the copyright holder to reuse or republish any previously published figures, illustrations, charts, tables, photographs, and text excerpts, etc. When submitting a manuscript, official written proof of permission must be provided and clearly stated in the cover letter.
The editorial office of the journal has the right to reject/retract articles that reuse third-party materials without permission.

Journal Policies on Data Sharing

We encourage authors to share articles published in our journal to other data platforms, but only if it is noted that it has been published in this journal.