Singular effects of Bacillus subtilis C-3102 or Saccharomyces cerevisiae type 1 on the growth, gut morphology, immunity, and stress resistance of red sea bream (Pagrus major)

Zaineldin, Amr I.; Hegazi, Sayed; Koshio, Shunsuke; Ishikawa, Manabu; Dawood, Mahmoud A.O.; Dossou, Serge; Yukun, Zhang; Mzengereza, Kumbukani

doi:10.2478/aoas-2020-0075

Abstract

The beneficial effects of Bacillus subtilis C-3102 and Saccharomyces cerevisiae type 1 were tested in red sea bream (Pagrus major) feeds. A basal diet (control) and two other diets were prepared by supplementation with B. subtilis C-3102 (PB) or S. cerevisiae type 1 (PY). After 60 days, both probiotic-supplemented groups exhibited significant enhancement in growth performance, the protein efficiency ratio (PER), and digestive enzyme secretion (protease and amylase) compared to the control group (P<0.05). The anterior, middle, and posterior parts of the intestines exhibited significantly increased values of intestinal fold height (hF), enterocyte height (hE), and microvillus height (hMV) in fish fed PB- or PY-supplemented diets (P<0.05). Serum peroxidase, anti-protease, and bactericidal activities were enhanced significantly in both probiotic-treated groups compared to the control group (P<0.05). Serum and mucus lysozyme activities improved significantly in the PB group compared to the control group (P<0.05). Catalase activity was also significantly decreased in both probiotic groups, with relatively lower activity observed in the PY group (P<0.05). Both probiotic groups showed considerably increased tolerance to freshwater exposure (P<0.05). In conclusion, B. subtilis C-3102 and S. cerevisiae type 1 can be used as functional probiotics to enhance the growth performance, digestion capacity, gut morphology, immune response, and stress resistance of the red sea bream with relatively higher efficiency by B. subtilis C-3102.

References

Abdel-Daim, M.M., Eissa, I.A.M., Abdeen, A., Abdel-Latif, H.M.R., Ismail, M., Dawood, M.A.O., Hassan, A.M. (2019). Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ. Toxicol. Pharmacol., 69: 44–50.
Search in Google Scholar Back to article
Adel, M., Yeganeh, S., Dawood, M.A.O., Safari, R., Radhakrishnan, S. (2017). Effects of Pediococcus pentosaceus supplementation on growth performance, intestinal microflora and disease resistance of white shrimp, Litopenaeus vannamei. Aquac. Nutr., 23: 1401–1409.
Search in Google Scholar Back to article
Akhter, N., Wu, B., Memon, A.M., Mohsin, M. (2015). Probiotics and prebiotics associated with aquaculture: a review. Fish Shellfish Immunol., 45: 733–741.
Search in Google Scholar Back to article
AOAC (2007). Method 2007-04. Association of Official Analytical Chemists. Washington, DC.
Search in Google Scholar Back to article
Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J., Struhl, K. (1998). Current protocols in molecular biology on CD-ROM. New York: John Wiley & Sons.
Search in Google Scholar Back to article
Ballerini, A., Civitareale, C., Fiori, M., Regini, M., Betti, M., Brambilla, G. (2003). Traceability of inbred and crossbred Cinta Senese pigs by evaluating the oxidative stress. J.Vet. Med. Ser. A., 50: 113–116.
Search in Google Scholar Back to article
Cao, Y., Liu, H., Qin, N., Ren, X., Zhu, B., Xia, X. (2020). Impact of food additives on the composition and function of gut microbiota: A review. Trends in Food Sci. Technol., 99: 295–310.
Search in Google Scholar Back to article
Carbone, D., Faggio, C. (2016). Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunol., 54: 172–178.
Search in Google Scholar Back to article
Cerezuela, R., Guardiola, F.A., González, P., Meseguer, J., Esteban, M.Á. (2012). Effects of dietary Bacillus subtilis, Tetraselmis chuii, and Phaeodactylum tricornutum, singularly or in combination, on the immune response and disease resistance of sea bream (Sparus aurata L.). Fish Shellfish Immunol., 33: 342–349.
Search in Google Scholar Back to article
Chiu, C.-H., Cheng, C.-H., Gua, W.-R., Guu, Y.-K., Cheng, W. (2010). Dietary administration of the probiotic, Saccharomyces cerevisiae P13 enhanced the growth, innate immune responses and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immunol., 29: 1053–1059.
Search in Google Scholar Back to article
Cupp-Enyard, C. (2008). Sigma’s non-specific protease activity assay-casein as a substrate. JoVE (Journal of Visualized Experiments), e899.10.3791/899287297719066538
Search in Google Scholar Back to article
Dawood M.A.O., Koshio S. (2016). Recent advances in the role of probiotics and prebiotics in carp aquaculture: A review. Aquaculture, 454: 243–251.
Search in Google Scholar Back to article
Dawood, M.A.O., Koshio, S., Ishikawa, M., Yokoyama, S. (2015). Effects of heat killed Lactobacillus plantarum (LP20) supplemental diets on growth performance stress resistance and immune response of red sea bream Pagrus major. Aquaculture, 442: 29–36.
Search in Google Scholar Back to article
Dawood, M.A.O., Koshio, S., Ishikawa, M., El-Sabagh, M., Esteban, M.A., 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.
Search in Google Scholar Back to article
Dawood, M.A.O., Koshio, S., El-Sabagh, M., Billah, M.M., Zaineldin, A.I., Zayed, M.M., Omar, A.A.E.-D. (2017). Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream Pagrus major. Aquaculture, 470: 214–222.
Search in Google Scholar Back to article
Dawood, M.A., Shukry, M., Zayed, M.M., Omar, A.A., Zaineldin, A.I., El Basuini, M.F. (2019a). Digestive enzymes, immunity and oxidative status of Nile tilapia (Oreochromis niloticus) reared in intensive conditions. Slov. Vet. Res., 56.
Search in Google Scholar Back to article
Dawood, M.A.O., Koshio, S., Abdel-Daim, M.M., Van Doan, H. (2019b). Probiotic application for sustainable aquaculture. Reviews in Aquac., 11: 907–924.10.1111/raq.12272
Search in Google Scholar Back to article
Dawood, M.A.O., Eweedah, N.M., Moustafa Moustafa, E., Shahin, M.G. (2019c). Effects of feeding regimen of dietary Aspergillus oryzae on the growth performance, intestinal morphometry and blood profile of Nile tilapia (Oreochromis niloticus). Aquac. Nutr., 25: 1063–1072.10.1111/anu.12923
Search in Google Scholar Back to article
De Los Santos, F.S., Donoghue, A., Farnell, M., Huff, G., Huff, W., Donoghue, D. (2007). Gastrointestinal maturation is accelerated in turkey poults supplemented with a mannan-oligosaccharide yeast extract (Alphamune). Poultry sci., 86: 921–930.
Search in Google Scholar Back to article
Dimitroglou, A., Merrifield, D., Moate, R., Davies, S., Spring, P., Sweetman, J., Bradley, G. (2009). Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout Oncorhynchus mykiss (Walbaum). J. Anim. Sci., 87: 3226–3234.
Search in Google Scholar Back to article
Dossou, S., Koshio, S., Ishikawa, M., Yokoyama, S., Dawood, M.A.O., El Basuini, M.F., Olivier, A., Zaineldin, A.I. (2018b). Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish Shellfish Immunol., 75: 253–262.10.1016/j.fsi.2018.01.03229360542
Search in Google Scholar Back to article
El Basuini, M.F., El-Hais, A.M., Dawood, M.A.O., Abou-Zeid, A.E.-S., EL-Damrawy, S.Z., Khalafalla, M.M.E.-S., Koshio, S., Ishikawa, M., Dossou, S. (2017). Effects of dietary copper nanoparticles and vitamin C supplementations on growth performance, immune response and stress resistance of red sea bream Pagrus major. Aquac. Nutr., 23: 1329–1340.
Search in Google Scholar Back to article
El-Boshy, M.E., Ahmed, M., AbdelHamid, F.M., Gadalla, H.A. (2010). Immunomodulatory effect of dietary Saccharomyces cerevisiae, β-glucan and laminaran in mercuric chloride treated Nile tilapia (Oreochromis niloticus) and experimentally infected with Aeromonas hydrophila. Fish Shellfish Immunol., 28: 802–808.
Search in Google Scholar Back to article
Ellis, A. (2001). Innate host defense mechanisms of fish against viruses and bacteria. Develop. Comp. Immunol., 25: 827–839.
Search in Google Scholar Back to article
Elsabagh, M., Mohamed, R., Moustafa, E.M., Hamza, A., Farrag, F., Decamp, O., Dawood, M.A.O., Eltholth, M. (2018). Assessing the impact of Bacillus strains mixture probiotic on water quality growth performance blood profile and intestinal morphology of Nile tilapia Oreochromis niloticus. Aquac. Nutr., 24: 1613–1622.
Search in Google Scholar Back to article
Faggio, C., Fedele, G., Arfuso, F., Panzera, M., Fazio, F. (2014). Haematological and biochemical response of Mugil cephalus after acclimation to captivity. Cahiers de Biol. Mar., 55: 31–36.
Search in Google Scholar Back to article
Gatesoupe, F. (1999). The use of probiotics in aquaculture. Aquaculture, 180: 147–165.
Search in Google Scholar Back to article
Geng, X., Dong, X.H., Tan, B.P., Yang, Q.H., Chi, S.Y., Liu, H.Y., Liu, X.Q. (2012). Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia Rachycentron canadum. Aquac. Nutr., 18: 46–55.
Search in Google Scholar Back to article
Gobi, N., Vaseeharan, B., Rekha, R., Vijayakumar, S., Faggio, C. (2018). Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotox. Environ. Saf., 162: 147–159.
Search in Google Scholar Back to article
Goth, L. (1991). A simple method for determination of serum catalase activity and revision of reference range. Clin. Chim. Acta, 196: 143–151.
Search in Google Scholar Back to article
Goth, L., Meszaros, I., Nemeth, H. (1982). Serum catalase enzyme activity in acute pancreatitis. Clin. Chem., 28: 1999–2000.
Search in Google Scholar Back to article
Guardiola, F., Porcino, C., Cerezuela, R., Cuesta, A., Faggio, C., Esteban, M. (2016). Impact of date palm fruits extracts and probiotic enriched diet on antioxidant status innate immune response and immune-related gene expression of European seabass (Dicentrarchus labrax). Fish Shellfish Immunol., 52: 298–308.
Search in Google Scholar Back to article
Hanif, A., Bakopoulos, V., Dimitriadis, G. (2004). Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish Shellfish Immunol., 17: 411–435.
Search in Google Scholar Back to article
He, S., Zhou, Z., Liu, Y., Shi, P., Yao, B., Ringø, E., Yoon, I. (2009a). Effects of dietary Saccharomyces cerevisiae fermentation product (DVAQUA®) on growth performance, intestinal autochthonous bacterial community and non-specific immunity of hybrid tilapia (Oreochromis niloticus ♀×O. aureus ♂) cultured in cages. Aquaculture, 294: 99–107.10.1016/j.aquaculture.2009.04.043
Search in Google Scholar Back to article
He, S., Zhou, Z., Liu, Y., Shi, P., Yao, B., Ringø, E., Yoon, I. (2009b). Effects of dietary Saccharomyces cerevisiae fermentation product (DVAQUA®) on growth performance, intestinal autochthonous bacterial community and non-specific immunity of hybrid tilapia (Oreochromis niloticus♀× O. aureus♂) cultured in cages. Aquaculture, 294: 99–107.10.1016/j.aquaculture.2009.04.043
Search in Google Scholar Back to article
Hooge, D., Ishimaru, H., Sims, M. (2004). Influence of dietary Bacillus subtilis C-3102 spores on live performance of broiler chickens in four controlled pen trials. J. Appl. Poult. Res., 13: 222–228.
Search in Google Scholar Back to article
Iida, Takahashi K, H, W. (1989). Decrease in the bactericidal activity of normal serum during the spawning period of rainbow trout. Nippon Suisan Gakkaishi, 55: 463–465.
Search in Google Scholar Back to article
Jeong, J., Kim, I. (2014). Effect of Bacillus subtilis C-3102 spores as a probiotic feed supplement on growth performance, noxious gas emission and intestinal microflora in broilers. Poultry Sci., 93: 3097–3103.
Search in Google Scholar Back to article
Kim, J.-H., Kang, J.-C. (2015). Oxidative stress neurotoxicity, and non-specific immune responses in juvenile red sea bream Pagrus major, exposed to different waterborne selenium concentrations. Chemosphere, 135: 46–52.
Search in Google Scholar Back to article
Kothari, D., Patel, S., Kim, S.-K. (2019). Probiotic supplements might not be universally-effective and safe: A review. Biomed. Pharmacol., 111: 537–547.
Search in Google Scholar Back to article
Kurtzman, C., Fell, J.W., Boekhout, T. (2011). The yeasts: a taxonomic study. Elsevier.
Search in Google Scholar Back to article
Li, P., Gatlin, I.D. (2004). Dietary brewers yeast and the prebiotic Grobiotic™ AE influence growth performance, immune responses and resistance of hybrid striped bass (Morone chrysops× M. saxatilis) to Streptococcus iniae infection. Aquaculture, 231: 445–456.
Search in Google Scholar Back to article
Liu, H., Wang, S., Cai, Y., Guo, X., Cao, Z., Zhang, Y., Liu, S., Yuan, W., Zhu, W., Zheng, Y. (2017). Dietary administration of Bacillus subtilis HAINUP40 enhances growth digestive enzyme activities, innate immune responses and disease resistance of tilapia Oreochromis niloticus. Fish Shellfish Immunol., 60: 326–333.
Search in Google Scholar Back to article
Lygren, B., Sveier, H., Hjeltnes, B., Waagbø, R. (1999). Examination of the immunomodulatory properties and the effect on disease resistance of dietary bovine lactoferrin and vitamin C fed to Atlantic salmon (Salmo salar) for a short-term period. Fish Shellfish Immunol., 9: 95–107.
Search in Google Scholar Back to article
Martínez Cruz, P., Ibáñez, A.L., Monroy Hermosillo, O.A., Ramírez Saad, H.C. (2012). Use of probiotics in aquaculture. ISRN Microbiol., 2012.10.5402/2012/916845367170123762761
Search in Google Scholar Back to article
Merrifield, D.L., Dimitroglou, A., Foey, A., Davies, S.J., Baker, R.T., Bøgwald, J., Castex, M., Ringø, E. (2010). The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture, 302: 1–18.
Search in Google Scholar Back to article
Merrifield, D., Bradley, G., Harper, G., Baker, R., Munn, C., Davies, S. (2011). Assessment of the effects of vegetative and lyophilized Pediococcus acidilactici on growth, feed utilization, intestinal colonization and health parameters of rainbow trout (Oncorhynchus mykiss Walbaum). Aquac. Nutr., 17: 73–79.
Search in Google Scholar Back to article
Moe, Y.Y., Koshio, S., Teshima, S.-i., Ishikawa, M., Matsunaga, Y., Panganiban Jr, A. (2004). Effect of vitamin C derivatives on the performance of larval kuruma shrimp, Marsupenaeus japonicus. Aquaculture, 242: 501–512.
Search in Google Scholar Back to article
Morganti, P., Bruno, C., Guarneri, F., Cardillo, A., Del Ciotto, P., Valenzano, F. (2002). Role of topical and nutritional supplement to modify the oxidative stress. I. J. Cosm. Sci., 24: 331–339.
Search in Google Scholar Back to article
Mustafa, A., Karmali, A., Abdelmoez, W. (2016). A sensitive microplate assay for lipase activity measurement using olive oil emulsion substrate: modification of the copper soap colorimetric method. J. Oleo. Sci., 65: 775–784.
Search in Google Scholar Back to article
Ortuño, J., Cuesta, A., Rodríguez, A., Esteban, M.A., 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.
Search in Google Scholar Back to article
Pasquini, A., Luchetti, E., Marchetti, V., Cardini, G., Iorio, E. (2008). Analytical performances of d-ROMs test and BAP test in canine plasma. Definition of the normal range in healthy Labrador dogs. Vet. Res. Com., 32: 137–143.
Search in Google Scholar Back to article
Peppler, H. (1982). Yeast extracts. Economic Microbiology ed. London: Academic Press.
Search in Google Scholar Back to article
Pinpimai, K., Rodkhum, C., Chansue, N., Katagiri, T., Maita, M., Pirarat, N. (2015). The study on the candidate probiotic properties of encapsulated yeast Saccharomyces cerevisiae JCM 7255, in Nile tilapia (Oreochromis niloticus). Res. Vet. Sci., 102: 103–111.
Search in Google Scholar Back to article
Pirarat, N., Pinpimai, K., Endo, M., Katagiri, T., Ponpornpisit, A., Chansue, N., Maita, M. (2011). Modulation of intestinal morphology and immunity in nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res. Vet. Sci., 91: e92–e97.
Search in Google Scholar Back to article
Ran, C., Huang, L., Liu, Z., Xu, L., Yang, Y., Tacon, P., Auclair, E., Zhou, Z. (2015). A comparison of the beneficial effects of live and heat-inactivated baker’s yeast on Nile tilapia: suggestions on the role and function of the secretory metabolites released from the yeast. Plos one, 10: e0145448.
Search in Google Scholar Back to article
Ringø, E., Doan, H.V., Lee, S.H., Soltani, M., Hoseinifar, S.H., Harikrishnan, R., Song, S.K. (2020). Probiotics, lactic acid bacteria and bacilli: interesting supplementation for aquaculture. J. Appl. Microbiol., https://doi.org/10.1111/jam.1462810.1111/jam.1462832141152
Search in Google Scholar Back to article
Salinas, I., Abelli, L., Bertoni, F., Picchietti, S., Roque, A., Furones, D., Cuesta, A., Meseguer, J., Esteban, M.Á. (2008). Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol., 25: 114–123.
Search in Google Scholar Back to article
Salma Zohora, U., Wahab Khan, A., Okanami, M., Ano, T., Shahedur Rahman, M. (2011). Study of submerged and biofilm fermentation of Bacillus subtilis using fish protein for production of lipopeptide antibiotic iturin A, Sci, Technology. Against Microb. Path., 190–195.10.1142/9789814354868_0037
Search in Google Scholar Back to article
Soltani, M., Ghosh, K., Hoseinifar, S.H., Kumar, V., Lymbery, A.J., Roy, S., Ringø, E. (2019). Genus bacillus, promising probiotics in aquaculture: Aquatic animal origin, bio-active components, bioremediation and efficacy in fish and shellfish. Rev. Fisher. Sci. Aquac., 27: 331–379.
Search in Google Scholar Back to article
Sun, Y.-Z., Yang, H.-L., Ma, R.-L., Lin, W.-Y. (2010). Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immunol., 29: 803–809.
Search in Google Scholar Back to article
Suzer, C., Çoban, D., Kamaci, H.O., Saka, Ş., Firat, K., Otgucuoğlu, Ö., 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.
Search in Google Scholar Back to article
Talpur, A.D., Munir, M.B., Mary, A., Hashim, R. (2014). Dietary probiotics and prebiotics improved food acceptability, growth performance, haematology and immunological parameters and disease resistance against Aeromonas hydrophila in snakehead (Channa striata) fingerlings. Aquaculture, 426: 14–20.
Search in Google Scholar Back to article
Tatsumi, N., Tsuji, R., Yamada, T., Kubo, K., Matsuda, T. (2000). Spot chem. EZ SP-4430 no kiso teki kento. J. Clin. Lab. Instr. Reag., 23: 427–433.
Search in Google Scholar Back to article
Terpou, A., Papadaki, A., Lappa, I.K., Kachrimanidou, V., Bosnea, L.A., Kopsahelis, N. (2019). Probiotics in food systems: Significance and emerging strategies towards improved viability and delivery of enhanced beneficial value. Nutrients, 11: 1591.
Search in Google Scholar Back to article
Van Doan, H., Hoseinifar, S.H., Ringø, E., Ángeles Esteban, M., Dadar, M., Dawood, M.A., Faggio, C. (2019). Host-associated probiotics: A key factor in sustainable aquaculture. Rev. Fisher.Sci. Aquac., 1–27.
Search in Google Scholar Back to article
Worthington, K. (2011). Worthington Enzyme Manual. Worthington Biochemical Corporation.
Search in Google Scholar Back to article
Yang, H.L., Sun, Y.Z., Ma, R.L., Ye, J.D. (2012). PCR-DGGE analysis of the autochthonous gut microbiota of grouper Epinephelus coioides following probiotic Bacillus clausii administration. Aquac.Res., 43: 489–497.
Search in Google Scholar Back to article
Zaineldin, A.I., Hegazi, S., Koshio, S., Ishikawa, M., Bakr, A., El-Keredy, A.M.S., Dawood, M.A.O., Dossou, S., Wang, W., Yukun, Z. (2018). Bacillus subtilis as probiotic candidate for red sea bream: Growth performance oxidative status and immune response traits. Fish Shellfish Immunol., 79: 303–312.
Search in Google Scholar Back to article

Singular effects of Bacillus subtilis C-3102 or Saccharomyces cerevisiae type 1 on the growth, gut morphology, immunity, and stress resistance of red sea bream (Pagrus major)

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