Abstract
Brewer’s spent yeast (BSY) is among the most voluminous by-products generated in brewery industry that adds to the waste; however, smart utilization of BSY could lead to edible biomass production besides waste management. To utilize it for biomass production, it is being used in fish feeds; however, its effect on the fish physiology has been scantily studied. The present study investigated the proteomic changes in muscle tissues of carp Labeo rohita fed with BSY-based diet, to understand its impact on muscle physiology and biomass. Six feeds were prepared with different grades of BSY (0, 20, 30, 40, 50, 100% replacement of fishmeal with BSY) and fishes were fed for 90 days. Highest weight gain%, feed conversion efficiency, specific growth rate% were observed in 30% BSY–replaced group and this group was considered for the proteomic study. Comparative shotgun proteomic analysis was carried out by LC–MS/MS and data generated have been deposited in ProteomeXchange Consortium with dataset identifier PXD020093. A total of 62 proteins showed differential abundance; 29 increased and 33 decreased in the 30% BSY–replaced group. Pathway analysis using IPA and Panther tools revealed that the proteins tyrosine protein kinase, PDGFα, PKRCB and Collagen promote muscle growth by inducing the PI3K-AKT pathway. Conversely, the proteins Serine/threonine-protein phosphatase, Phosphatidylinositol 3,4,5-trisphosphate5-phosphatase 2A and Ras-specific guanine- nucleotide-releasing factor inhibit muscle growth indicating that 30% BSY–replaced feed promote muscle growth in a highly controlled manner. Findings suggest that BSY could be recycled for carp feed production in large scale thereby leading to resource conservation, reducing environmental effects.
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Data availability
Proteomic data generated in this study have been deposited in ProteomeXchange Consortium with dataset identifier PXD020093.
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Not applicable.
References
Abowei JFN, Ekubo AT (2011) A review of conventional and unconventional feeds in fish nutrition. Br J Pharmacol Toxicol 2:179–191
AOAC (2012) Official Methods of Analysis. 18th Arlington, VA, USA: Association of Official Analytical Chemists International.
Blaauw B (2017) Platelet- Derived Growth Factor signaling and the role of cellular crosstalk in functional muscle growth. FEBS Lett 591:690–692
Beesigamukama D, Mochoge B, Korir NK, Fiaboe KKM, Nakimbugwe D, Khamis FM, Subramanian S, Wangu MM, Dubois T, Ekesi S, Tanga CM (2021) Low-cost technology for recycling agro-industrial waste into nutrient-rich organic fertilizer using black soldier fly. Waste Manag 119:183–194
Craig S, Helfrich LA (2002) Understanding fish nutrition, feeds and feeding. Virginia State University, USA, Cooperative Extension Service, pp 420–256
Das P, Sahoo L, Das SP, Bit A, Joshi CG et al (2020) De novo assembly and genome-wide SNP discovery in rohu carp. Labeo Rohita Front Genet 11:386
Doessing S, Heinemeier KM, Holm L, Mackey AL, Schjerling P, Rennie M, Kenneth S, Reitelseder S, Kappelgaard AM, Rasmussen MH, Flyvbjerg A, Kjaer M (2010) Growth hormone stimulates the collagen synthesis in human tendon and skeletal muscle without affecting myofibrillar protein synthesis. J Physiol 588:341–351
Dorothy MS, Raman S, Nautiyal V, Singh K, Yogananda T, Kamei M (2018) Use of potential plant leaves as ingredient in fish feed-a review. Int J Curr Microbiol App Sci 7(7):112–125
Doupé G, Lymbery AJ (2007) Toward the genetic improvement of feed conversion efficiency in fish. J World Aqua Soc 34(3):245–254
Duncan DB (1955) Multiple range and multiple F-tests. Biometrics 11:1–42
FAO (2014) The State of World Fisheries & Agriculture Organization of the United Nations. Italy, Rome
FAO (2020a) Cultured Aquatic Species Information Programme: Labeo rohita (Hamilton, 1822)http://www.fao.org/fishery/culturedspecies/Labeo_rohita/en#:~:text=The%20latter%20type%20of%20aquaculture,70%20percent%20of%20the%20stock
FAO (2020b) The State of World Fisheries and Aquaculture 2020. Sustainability in action, Rome. https://doi.org/10.4060/ca9229en
Ghamkhar R, Hicks A (2020) Comparative environmental impact assessment of aquafeed production: sustainability implications of forage fish meal and oil free diets. Resource Conserv Recycl 161:104849
Gumus E, Aydin B, Kanyilmaz M (2016) Growth and fed utilization of goldfish (Carassius auratus) fed graded levels of brewer’s yeast (Saccharomyces cerevisiae). Ind J Fish Sci 15(3):1124–1133
ICAR (2020) First report of rohu induced breeding in November. https://icar.org.in/node/5651
Jacob FF, Striegel L, Rychlik M, Mathias H, Methner FJ (2019) Spent yeast from brewing processes: a biodiverse starting material for yeast extract production. Fermentation 5:51
Jannathulla R, Rajaram V, Kalanjiam R, Ambasankar K, Muralidhar M, Dayal JS (2019) Fishmeal availability in the scenarios of climate change: inevitability of fishmeal replacement in aquafeeds and approaches for the utilization of plant protein sources. Aquacult Res 50(12):3493–3506
Jayant M, Hassan MA, Srivastava PP, Meena DK, Kumar P, Kumar A, Wagde MS (2018) Brewer’s spent grains (BSGs) as feedstuff for striped catfish, Pangasianodon hypophthalmus fingerlings: an approach to transform waste into wealth. J Clean Prod 199, 716e722.
Kaur VI, Saxena PK (2004) Incorporation of brewery waste in supplementary feed and its impact on growth of some carps. Biores Technol 91:101–104
Kerby C, Vriesekoop F (2017) An overview of the utilisation of brewery by-products as generated by british craft breweries. Beverages 3:24
Korkmaz AS, Cakirogullari GC (2011) Effects of partial replacement of fish meal by dried baker’s yeast (Saccharomyces cerevisiae) on growth performance, feed utilization and digestibility in koi carp (Cyprinus carpio L., 1758) fingerlings. J Animal Vet Adv 10:346–351
Lifeyeast.com, 2019. Recycling brewer´spent yeast in innovative industrial applications. Accessed on 16–1–2022.
Martin DS, Orive M, Inarra B, Castelo J, Estevez A, Nazzaro J, Iloro I, Elortza F, Zufia J (2020) Brewers’ spent yeast and grain protein hydrolysates as second-generation feedstuf for aquaculture feed. Waste Biomass Valor. https://doi.org/10.1007/s12649-020-01145-8
Mathias TRS, de Mello PPM, Servulo EFC (2014) Solid wastes in brewing process: a review. Journal Brew Distilling 5:1–9
Miao W, Wang W (2020) Trends of aquaculture production and trade: carp, tilapia and shrimp. Asian Fish Sci 33:1–10
Mishra K, Samanataray K (2004) Interacting effects of dietary lipid level and temperature on growth, body composition and fatty acid profile of rohu, Labeo rohita (Hamilton). Aquacult Nutr 10:359–369
Mohanty BP, Mahanty A, Ganguly S, Mitra T, Karunakaran D, Anandan R (2019) Nutritional composition of food fishes and their importance in providing food and nutritional security. Food Chem 293:561–570
Mzengereza K, Msiska OV, Kapute F, Kang’ombe J, Singini W, Kamangira A (2014) Nutritional value of locally available plants with potential for diets of Tilapia rendalli in pond aquaculture in NkhataBay. Malawi J Aquacult Res Dev 5:265
Nguyen NHY, Trinh LT, Chau DT, Baruah K, Lundh T, Kiessling A (2019) Spent brewer’s yeast as a replacement for fishmeal in diets for giant freshwater prawn (Macrobrachium rosenbergii), reared in either clear water or a biofloc environment. Aquacult Nutr 25:970–979
Oliva-Teles A, Goncalves P (2001) Partial replacement of fishmeal by brewer’s yeast (Saccaromyces cerevisae) in diets for sea bass (Dicentrarchus labrax) juveniles. Aquacult 202:269–278
Ozorio ROA, Portz L, Borghesi R, Cyrino JEP (2012) Effects of dietary yeast (Saccharomyces cerevisiae) supplementation in practical diets of tilapia (Oreochromis niloticus). Animals 2:16–24
Ozorio ROA, Turini BGS, Moro GV, Oliveira LST, PORTZ L, Cyrino JEP, (2010) Growth, nitrogen gain and indispensable amino acid retention of pacu (Piaractus mesopotamicus, Holmberg 1887) fed different brewer’s yeast (Saccharomyces cerevisiae) levels. Aqua Nutr 16:276–283
Pell JM, Bates PC (1987) Collagen and non–collagen protein turnover in skeletal muscle of growth hormone–treated lambs. J Endocrin 115:R1–R4
Peng D, Liang XF, Chai F, Feng H, Li J, Tang S, Lu K, Zhang Q (2022) Effects of dietary carbohydrate to lipid ratios on growth, biochemical indicators, lipid metabolism, and appetite in Chinese perch (Siniperca chuatsi). Fish Physiol Biochem 48:101–116
Rl P, Brown ML (1967) Nutrition: an integrated approach. Wiley, New York, p 542
Ramakrishna R, Shipton TA, Hasan MR (2013) Feeding and feed management of Indian major carps in Andhra Pradesh, India. FAO Fisheries and Aquaculture Technical Paper No. 578. Rome, FAO. 90 pp.
Ribeiro-Oliveira R, Martins ZE, Sousa JB, Ferreira MPLVOI, Diniz C (2021) The health-promoting potential of peptides from brewing by-products: an up-to-date review. Trend Food Sci Technol 118:143–153
Reed G, Nagodawithana TW (1991) Yeast technology, AVI-Van Nostrand Reinhold, New York, NY, USA.
Reyhani V, Tsioumpekou M, Wieringen T, Rask L, Lennartsson V, Rubin K (2017) PDGF-BB enhances collagen gel contraction through a PI3K-PLCγ-PKC-cofilin pathway. Sci Rep 7:8924
Rumsey GL, Kinsella JE, Shetty KJ, Hughes SG (1991) Effect of high dietary concentrations of brewer’s dried yeast on growth performance and liver uricase in rainbow trout (Oncorhynchus mykiss). Ani Feed Sci Technol 33:177–183
Salin KR, Arun VV, Nair CM, Tidwell JH (2018) Sustainable aquafeed, part of sustainable aquaculture in applied environmental science and engineering for a sustainable future. Springer, Cham, Switzerland
Samantaray K, Mohanty SS (1997) Interactions of dietary levels of protein and energy on fingerling Snakehead, Channa striata. Aquacult 156:241–249
Sandre LCG, Buzallo H, Nascimento TMT, Neira LM, Jomori RK, Carmeiro DJ (2017) Productive performance and digestibility in the initial growth phase of tambaqui (Colossoma marcopomum) fed diets with different carbohydrate and lipid levels. Aquacult Rep 6:28–34
Solomon SG, Ataguba GA, Itodo GE (2017) Performance of Clarias gariepinus fed dried brewer’s yeast (Saccharomyces cerevisiae) slurry in replacement for soybean meal. J Nutr Metab 2017, Article ID 8936060, 8 pages.
Sugg KB, Korn MA, Sarver DC, Markworth JF, Mendias CL (2017) Inhibition of platelet-derived growth factor signaling prevents muscle fiber growth during skeletal muscle hypertrophy. FEBS Lett 591:801–809
Tanguler H, Erten H (2008) Utilisation of spent brewer’s yeast for yeast extract production by autolysis: the effect of temperature. Food Bioprod Process 86:317–321
UNDP, 2015. UNDP Sustainable development goals responsible consumption and production. https://www.undp.org/content/undp/en/home/sustainable-development-goals/goal-12-responsible-consumption-and-production.html#targets. Accessed on 1 5.1.2022
Valente LMP, Moutou KA, Conceicao LEC, Engrola S, Fernandes JMO, Johnston IA (2013) What determines growth potential and juvenile quality of farmed fish species? Rev Aquacult 5(Suppl. 1):S168–S193
Vieira EF, Carvalho J, Pinto E, Cunha S, Almeida AA, Ferreira IMPLVO (2016) Nutritive value, antioxidant activity and phenolic compounds profile of brewer’s spent yeast extract. J Food Comp Anal 52:44–51
Yuan XY, Jiang GZ, Wang CC, Abasubong KP, Zou Q, Zhou YY, Liu WB (2019) Effects of partial replacement of fish meal by yeast hydrolysate on antioxidant capability, intestinal morphology, and inflammation-related gene expression of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 45:187–197
Elia D, Madhala D, Ardon E, Reshef R, Halev O (2007) Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta 1773:1438–1446
Fuentes E, Björnsson BT, Valdés J, Einarsdottir I, Lorca B, Alvarez M, Molina A (2011) IGF-. Comp Physiol 300:1532–1542
Yang S, Liu Z, Yan Z, Zhao Z, Zhang C, Gong Q, Du X, Wu J, Feng Y, Du J, Huang X (2021) Improvement of skeletal muscle growth by GH/IGF growth-axis contributes to growth performance in commercial fleshy sturgeon. Aquacult 543:736929
Palstra AA, Rovira M, Rizo-Roca D, Torrella JR, Spaink HP, Planas JV (2014) Swimming-induced exercise promotes hypertrophy and vascularization of fast skeletal muscle fibres and activation of myogenic and angiogenic transcriptional programs in adult zebrafish. BMC Genomics 15:1136
Li L, Blumenthal DK, Terry CM, He Y, Carlson ML, Cheung AK (2010) PDGF-induced proliferation in human arterial and venous smooth muscle cells: Molecular basis for differential effects of PDGF isoforms. J Cell Biochem 112(1):289–298
Rohde HM, Cheong FY, Konrad G, Paiha K, Mayinger P, Boehmelt G (2003) The human phosphatidylinositol phosphatase SAC1 interacts with the coatomer I complex. J Biol Chem 278(52):52689–52699
Thota SG, Unnikannan CP, Thampatty SR, Manorama R, Bhandari R (2015) Inositol pyrophosphates regulate RNA polymerase I-mediated rRNA transcription in Saccharomyces cerevisiae. Biochem J 466(1):105–114
Morita M, Ler LW, Fabian MR, Siddiqui N, Mullin M, Henderson V et al (2012) A novel 4EHP-GIGYF2 translational repressor complex is essential for mammalian development. Mol Cell Biol 32(17):3585–3593
Funding
KS is an Emeritus Professor at ICAR—Central Institute of Freshwater Aquaculture (CIFA), Bhubaneswar. The Indian Council of Agricultural Research supported this study under Emeritus Professor Scheme to KS. The study was also partly supported by ICAR through core-funding to CIFRI, Barrackpore (BPM). The authors (KS, DP) are thankful to the Director, CIFA, Bhubaneswar, for the facilities and encouragement.
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DP—experimental study, maintaining experimental animals, feed design, feeding trial and data analysis, manuscript preparation. AM—feeding trial, proteomic study, proteomic data analysis, data deposition, manuscript preparation and review. SM—proteomic study and proteomic data analysis, manuscript review. KS—conceptualization, funding, guidance, feed design, feeding trial and data analysis, manuscript preparation and review. BPM—conceptualization, funding, guidance, proteomic study and proteomic data analysis, manuscript preparation and review. All authors read and approved the final manuscript.
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Pradhan, D., Mahanty, A., Mohanty, S. et al. Brewer’s spent yeast replacement in carp diet leads to muscle biomass production, recycling, waste management and resource conservation. Fish Physiol Biochem 48, 1427–1442 (2022). https://doi.org/10.1007/s10695-022-01133-w
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DOI: https://doi.org/10.1007/s10695-022-01133-w