Tilapia viscera wastewater: an innovative substrate for sustainable biosurfactant production by Penicillium citrinum UCP 1183

Everton Ricardo Carneiro Costa; Dayana Montero Rodríguez; Adriana  Ferreira de Souza; Galba Maria de Campos-Takaki; Rosileide Fontenele da Silva Andrade

doi:10.5327/Z2176-94782524

Authors

Everton Ricardo Carneiro Costa Universidade Católica de Pernambuco (UNICAP) - Brazil https://orcid.org/0000-0002-4132-9350
Dayana Montero Rodríguez Universidade Católica de Pernambuco (UNICAP) - Brazil https://orcid.org/0000-0001-8954-7309
Adriana Ferreira de Souza Universidade Católica de Pernambuco (UNICAP) - Brazil https://orcid.org/0000-0002-9527-2206
Galba Maria de Campos-Takaki Universidade Católica de Pernambuco (UNICAP) - Brazil https://orcid.org/0000-0002-0519-0849
Rosileide Fontenele da Silva Andrade Universidade Católica de Pernambuco (UNICAP) - Brazil https://orcid.org/0000-0001-8526-554X

DOI:

https://doi.org/10.5327/Z2176-94782524

Keywords:

fish processing waste; fungal surfactant; emulsifying properties.

Abstract

Sustainable fish waste management is a critical issue linked to the United Nations Sustainable Development Goals, particularly SDG 12 (Sustainable Consumption and Production). Improper disposal of fish processing residues, including viscera, causes significant environmental problems by worsening pollution and wasting valuable biotechnological resources. In order to contribute to the solution of this economic and environmental challenge, this study sought to use wastewater from the processing of Nile tilapia (Oreochromis niloticus) viscera as a raw material for biosurfactant production by Penicillium citrinum UCP 1183. This strain was cultivated in alternative media composed of tilapia viscera wastewater and post-frying soybean oil, based on the concentrations established by a 22 full-factorial design. Biosurfactant production was verified in condition 4 of the full-factorial design, obtaining a surface tension of 36 mN/m. The biosurfactant showed an anionic and lipopeptide nature, moderate zeta potential, and excellent stability and emulsifying capacity. Hence, tilapia viscera wastewater proved to be an excellent substrate for sustainable biosurfactant production, minimizing the environmental impact of fish processing waste and promoting the circular economy.

Downloads

Download data is not yet available.

References

Alexandre, A.C.S.; Albergaria, F.C.; Fernandes, L.A.C.; de Sousa Gomes, M.E.; Pimenta, C.J., 2022. Effect of natural and synthetic antioxidants on oxidation and storage stability of mechanically separated tilapia meat. LWT, v. 154, 112679. https://doi.org/10.1016/j.lwt.2021.112679.

Arias, L.; Marquez, D.M.; Zapata, J.E., 2022. Quality of red tilapia viscera oil (Oreochromis sp.) as a function of extraction methods. Heliyon, v. 8 (5), e09546. https://doi.org/10.1016/j.heliyon.2022.e09546.

Barbosa, J.C.; Gonçalves, S.; Makowski, M.; Silva, I.C.; Caetano, T.; Schneider, T.; Mösker, E.; Süssmuth, R.D.; Santos, N.C.; Mendo, S., 2022. Insights into the mode of action of the two-peptide lantibiotic lichenicidin. Colloids and Surfaces B: Biointerfaces, v. 211, 112308. https://doi.org/10.1016/j.colsurfb.2021.112308.

Bjerk, T.R.; Severino, P.; Jain, S.; Marques, C.; Silva, A.M.; Pashirova, T.; Souto, E.B., 2021. Biosurfactants: properties and applications in drug delivery, biotechnology, ecotoxicology. Bioengineering, v. 8 (8), 115. https://doi.org/10.3390/bioengineering8080115.

Borges, S.; Odila, J.; Voss, G.; Martins, R.; Rosa, A.; Couto, J.A.; Almeida, A.; Pintado, M., 2023. Fish by-products: a source of enzymes to generate circular bioactive hydrolysates. Molecules, v. 28 (3), 1155. https://doi.org/10.3390/molecules28031155.

Camargo-de-Morais, M.M.; Ramos, S.A.F.; Pimentel, M.C.B.; de Morais Jr, M.A.; Lima Filho, J.L., 2003. Production of an extracellular polysaccharide with emulsifier properties by Penicillium citrinum. World Journal of Microbiology and Biotechnology, v. 19, 191-194. https://doi.org/10.1023/A:1023299111663.

Castor, R.B.; do Nascimento, M.H.; Gorlach-Lira, K., 2024. Exploring fungal bioemulsifiers: insights into chemical composition, microbial sources, and cross-field applications. World Journal of Microbiology and Biotechnology, v. 40 (4), 127. https://doi.org/10.1007/s11274-024-03883-6.

Cavenaghi-Altemio, A.D.; Zitkoski, J.L.; Fonseca, G.G., 2022. Development and characterisation of cooked inlaid sausages with fillet and mechanically separated meat of Nile tilapia (Oreochromis niloticus). Journal of Fisheries, v. 10 (2), 102207. https://doi.org/10.17017/j.fish.437.

Chabhadiya, S.; Acharya, D.K.; Mangrola, A.; Shah, R.; Pithawala, E.A., 2024. Unlocking the potential of biosurfactants: innovations in metabolic and genetic engineering for sustainable industrial and environmental solutions. Biotechnology Notes. https://doi.org/10.1016/j.biotno.2024.07.001.

Chauhan, S.; Mohanty, A.; Meena, S.S., 2025. Unlocking the potential of rhamnolipids: production via agro-industrial waste valorization, market insights, recent advances, and applications. Biomass Conversion and Biorefinery, 1-30. https://doi.org/10.1007/s13399-025-06671-w

Cooper, D.G.; Goldenberg, B.G., 1987. Surface-active agents from two Bacillus species. Applied and Environmental Microbiology, v. 53 (2), 224-229. https://doi.org/10.1128/aem.53.2.224-229.1987.

Costa, E.R.C.; Souza, A.F.; de Campos Takaki, G.M.; da Silva Andrade, R.F., 2023. Bioemulsifier production by Penicillium citrinum UCP 1183 and microstructural characterization of emulsion droplets. Seven Editora,São José dos Pinhais. https://doi.org/10.56238/Connnexpemultidisdevolpfut-168.

Dabaghi, S.; Ataei, S.A.; Taheri, A., 2023. Production of rhamnolipid biosurfactants in solid-state fermentation: process optimization and characterization studies. BMC Biotechnology, v. 23 (1), 2. https://doi.org/10.1186/s12896-022-00772-4.

D'Almeida, A.P.; de Albuquerque, T.L.; Rocha, M.V.P., 2024. Recent advances in Emulsan production, purification, and application: exploring bioemulsifiers unique potentials. International Journal of Biological Macromolecules, v. 278 (Part 1), 133672. https://doi.org/10.1016/j.ijbiomac.2024.133672.

Dini, S.; Bekhit, A.E.D.A.; Roohinejad, S.; Vale, J.M.; Agyei, D., 2024. The physicochemical and functional properties of biosurfactants: a review. Molecules, v. 29 (11), 2544. https://doi.org/10.3390/molecules29112544.

Gautam, G.; Mishra, V.; Verma, P.; Pandey, A.K.; Negi, S., 2014. A cost effective strategy for production of bio-surfactant from locally isolated Penicillium chrysogenum SNP5 and its applications. Journal of Bioprocessing and Biotechniques, v. 4 (6), 1-7. https://doi.org/10.4172/2155-9821.1000177.

Gautam, K.; Sharma, P.; Gaur, V.K.; Gupta, P.; Pandey, U.; Varjani, S.; Pandey, A.; Wong, J.W.C.; Chang, J.S., 2023. Oily waste to biosurfactant: a path towards carbon neutrality and environmental sustainability. Environmental Technology Innovation, v. 30, 103095. https://doi.org/10.1016/j.eti.2023.103095.

Gayathiri, E.; Prakash, P.; Karmegam, N.; Varjani, S.; Awasthi, M.K.; Ravindran, B., 2022. Biosurfactants: potential and eco-friendly material for sustainable agriculture and environmental safety - a review. Agronomy, v. 12 (3), 662. https://doi.org/10.3390/agronomy12030662.

He, H.; Cao, M.; Zhan, D.; Xia, W.; Chen, S.; Tao, X.; Huang, Z., 2023. Preliminary study on the surface modification of lignite and bioflotation by white-rot fungi Hypocrea lixii AH. Minerals, v. 13 (12), 1492. https://doi.org/10.3390/min13121492.

Jasrotia, R.; Langer, S.; Dhar, M., 2024. Fish Waste and By-Product Utilization: a circular economy. In: Maqsood, S.; Naseer, M.N.; Benjakul, S.; Zaidi, A.A. Fish waste to valuable products. Springer Nature Singapore, Singapore, pp. 461-477. https://doi.org/10.1007/978-981-99-8593-7_22

Jimenez-Champi, D.; Romero-Orejon, F.L.; Muñoz, A.M.; Ramos-Escudero, F., 2024. The revalorization of fishery by‐products: types, bioactive compounds, and food applications. International Journal of Food Science, v. 2024 (1), 6624083. https://doi.org/10.1155/2024/6624083.

Kazemzadeh, S.; Emami‐Karvani, Z.; Naghavi, N.S.; Emtiazi, G., 2022. Production of surface‐active sophorolipid biosurfactant and crude oil degradability by novel Rhodotorula mucilaginosa strain SKF2. Journal of Surfactants and Detergents, v. 25 (4), 439-454. https://doi.org/10.1002/jsde.12572.

Klahan, R.; Yuangsoi, B.; Whangchai, N.; Ramaraj, R.; Unpaprom, Y.; Khoo, K.S.; Deepanraj, B. Pimpimol, T., 2023. Biorefining and biotechnology prospects of low-cost fish feed on Red tilapia production with different feeding regime. Chemosphere, v. 311, 137098. https://doi.org/10.1016/j.chemosphere.2022.137098.

Kuley, E.; Özyurt, G.; Özogul, I.; Boga, M.; Akyol, I.; Rocha, J.M.; Özogul, F., 2020. The role of selected lactic acid bacteria on organic acid accumulation during wet and spray-dried fish-based silages. Contributions to the winning combination of microbial food safety and environmental sustainability. Microorganisms, v. 8 (2), 172. https://doi.org/10.3390/microorganisms8020172.

Kumar, V.; Kumar, H.; Vishal, V.; Lal, S., 2023. Studies on the morphology, phylogeny, and bioremediation potential of Penicillium citrinum and Paecilomyces variotii (Eurotiales) from oil-contaminated areas. Archives of Microbiology, v. 205 (1), 50. https://doi.org/10.1007/s00203-022-03383-x.

Kupikowska-Stobba, B.; Domagała, J.; Kasprzak, M.M., 2024. Critical review of techniques for food emulsion characterization. Applied Sciences, v. 14(3), 1069. https://doi.org/10.3390/app14031069.

Kuyukina, M.S.; Ivshina, I.B.; Makarov, S.O.; Litvinenko, L.V.; Cunningham, C.J.; Philp, J.C., 2005. Effect of biosurfactants on crude oil desorption and mobilization in a soil system. Environment International, v. 31 (2), 155-161. https://doi.org/10.3390/microorganisms8020172.

Landa-Faz, A.; Rodríguez-Vázquez, R.; Roldán-Carrillo, T.G.; Hidalgo-Lara, M.E.; Aguilar-López, R.; Cebrián-García, M.E., 2022. Bioremediation of an agricultural saline soil contaminated with endosulfan and Escherichia coli by an active surface agent induced in a Penicillium crustosum culture. Preparative Biochemistry Biotechnology, v. 52 (3), 292-301. https://doi.org/10.1080/10826068.2021.1941104

Lee, T.C.; Pu'ad, N.M.; Alipal, J.; Muhamad, M.S.; Basri, H.; Idris, M.I.; Abdullah, H.Z., 2022. Tilapia wastes to valuable materials: a brief review of biomedical, wastewater treatment, and biofuel applications. Materials Today: Proceedings, v. 57, 1389-1395. https://doi.org/10.1016/j.matpr.2022.03.174.

Liepins, J.; Balina, K.; Soloha, R.; Berzina, I.; Lukasa, L.K.; Dace, E., 2021. Glycolipid biosurfactant production from waste cooking oils by yeast: review of substrates, producers and products. Fermentation, v. 7 (3), 136. https://doi.org/10.3390/fermentation7030136.

Lima, R.A.; Andrade, R.F.; Rodríguez, D.M.; Araujo, H.W.; Santos, V.P.; Campos-Takaki, G.M., 2017. Production and characterization of biosurfactant isolated from Candida glabrata using renewable substrates. African Journal of Microbiology Research, v. 11, 237-244. https://doi.org/10.5897/AJMR2016.8341.

Lima, B.G.; Santos, J.C.; Silva, R.R.; Caldas, M.C.F.; Meira, H.M.; Rufino, R.D.; Sarubbo, L.A. Luna, J.M., 2024. Sustainable production of biosurfactant grown in medium with industrial waste and use for removal of oil from soil and seawater. Surfaces, v. 7 (3), 537-549. https://doi.org/10.3390/surfaces7030036.

Luft, L.; Confortin, T.C.; Todero, I.; Zabot, G.L.; Mazutti, M.A., 2020. An overview of fungal biopolymers: bioemulsifiers and biosurfactants compounds production. Critical Reviews in Biotechnology, v. 40 (8), 1059-1080. https://doi.org/10.1080/07388551.2020.1805405.

Maksimenko, A.; Belyi, L.; Podvolotskaya, A.; Son, O.; Tekutyeva, L., 2024. Exploring sustainable aquafeed alternatives with a specific focus on the ensilaging technology of fish waste. Fermentation, v. 10 (5), 258. https://doi.org/10.3390/fermentation10050258.

Montoya, J.E.Z.; Sanchez, A.F., 2022. The hydrolysates from fish by-product, an opportunity increasing. Hydrolases, v. 77, 95149. https://doi.org/10.5772intechopen.95149.

Mozumder, M. M. H.; Uddin, M. M.; Schneider, P.; Raiyan, M. H. I.; Trisha, M. G. A.; Tahsin, T. H.; Newase, S., 2022. Sustainable utilization of fishery waste in Bangladesh—a qualitative study for a circular bioeconomy initiative. Fishes, v. 7 (2), 84. https://doi.org/10.3390/fishes7020084

Naumann, D., 2000. Infrared spectroscopy in microbiology, In: Meyers, R.A. (Ed.), Encyclopedia of Analytical Chemistry. John Wiley Sons Ltd, Chichester, U.K., p. 102.

Olivia, R.; Ang, C.H.; Clotilda, P.; Caroline, M.; Rudy, T.; Joe, N., 2023. Corrosion inhibition of mild steel bars by biosurfactant produced by Penicillium citrinum. IOP Conference Series: Earth and Environmental Science, v. 1135 (1), 012057. https://doi.org/10.1088/1755-1315/1135/1/012057.

Othman, A.R. ; Ismail, N.S.; Abdullah, S.R.S.; Hasan, H.A.; Kurniawan, S.B.; Sharuddin, S.S.N.; Ismail, N.‘I., 2022. Potential of indigenous biosurfactant-producing fungi from real crude oil sludge in total petroleum hydrocarbon degradation and its future research prospects. Journal of Environmental Chemical Engineering, v. 10 (3), 107621. https://doi.org/10.1016/j.jece.2022.107621.

Pathania, A.S.; Jana, A.K.; Jana, M.M., 2021. Valorization of waste frying oil to lipopeptide biosurfactant by indigenous Bacillus licheniformis through co-utilization in mixed substrate fermentation. Brazilian Journal of Chemical Engineering, v. 39, 369-385. https://doi.org/10.1007/s43153-021-00170-x.

Ponsano, E.H.G.; Grassi, T.L.M.; Santo, E.F.E.; de Lima, L.K.F.; Pereira, R.D.C., 2019. Production and use of microbial biomass helping sustainability in tilapia production chain. 3 Biotech, v. 9 (9), 325. https://doi.org/10.1007/s13205-019-1860-z.

Purwasena, I.A.; Amaniyah, M.; Astuti, D.I.; Firmansyah, Y.; Sugai, Y., 2024. Production, characterization, and application of Pseudoxanthomonas taiwanensis biosurfactant: a green chemical for microbial enhanced oil recovery (MEOR). Scientific Reports, v. 14 (1), 10270. https://doi.org/10.1038/s41598-024-61096-1.

Rajabimashhadi, Z.; Gallo, N.; Salvatore, L.; Lionetto, F., 2023. Collagen derived from fish industry waste: progresses and challenges. Polymers, v. 15 (3), 544. https://doi.org/10.3390/polym15030544

Rasmiya Begum, S.L.; Himaya, S.M.M.S.; Imthiyas, M.S.M.; Afreen, S.M.M.S., 2024. Fish waste: understanding the pollution potential and sustainable mitigation strategies. In: Maqsood, S.; Naseer, M.N.; Benjakul, S.; Zaidi, A.A. Fish waste to valuable products. Springer Nature Singapore, Singapore, pp. 427-440. https://doi.org/10.1007/978-981-99-8593-7_20.

Rifna, E J.; Rajauria, G.; Dwivedi, M.; Tiwari, B.K., 2024. Circular economy approaches for the production of high-value polysaccharides from microalgal biomass grown on industrial fish processing wastewater: a review. International Journal of Biological Macromolecules, v. 254, 126887.

Sanches, R.A.; Mendes, F.D.; de Campos Araújo, M.; Issac, M.G., 2024. Textile waste is the raw material for new fashion products. In: Raposo, D.; Neves, J.; Silva, R. Perspectives on Design III: Research, Education and Practice. Springer Nature Switzerland, Cham, pp. 297-310. https://doi.org/10.1007/978-3-031-43516-4_17.

Sankhyan, S.; Kumar, P.; Pandit, S.; Kumar, S.; Ranjan, N.; Ray, S., 2024. Biological machinery for the production of biosurfactant and their potential applications. Microbiological Research, v. 285, 127765. https://doi.org/10.1016/j.micres.2024.127765.

Santana, T.M.; Dantas, F.D.M.; Monteiro Dos Santos, D.K.; Kojima, J.T.; Pastrana, Y. M.; De Jesus, R.S.; Gonçalves, L.U., 2023. Fish viscera silage: production, characterization, and digestibility of nutrients and energy for tambaqui juveniles. Fishes, v. 8 (2), 111. https://doi.org/10.3390/fishes8020111.

Sar, T.; Ferreira, J.A.; Taherzadeh, M.J., 2021. Conversion of fish processing wastewater into fish feed ingredients through submerged cultivation of Aspergillus oryzae. Systems Microbiology and Biomanufacturing, v. 1, 100-110. https://doi.org/10.1007/s43393-020-00009-5.

Sharma, J.; Kapley, A.; Sundar, D.; Srivastava, P., 2022. Characterization of a potent biosurfactant produced from Franconibacter sp. IITDAS19 and its application in enhanced oil recovery. Colloids and Surfaces B: Biointerfaces, v. 214, 112453. https://doi.org/10.1016/j.colsurfb.2022.112453.

Silva, A.F.; Banat, I.M.; Giachini, A.J.; Robl, D., 2021. Fungal biosurfactants, from nature to biotechnological product: bioprospection, production and potential applications. Bioprocess and Biosystems Engineering, v. 44 (10), 2003-2034. https://doi.org/10.1007/s00449-021-02597-5.

Soliman, M.A.; Khedr, A.; Elsawy, M.A., 2023. Peptide and protein emulsifiers. In: Elsawy, M.A. Peptide bionanomaterials: from design to application. Springer International Publishing, Cham, pp. 431-474. https://doi.org/10.1007/978-3-031-29360-3_13

Suseno, S.H.; Rizkon, A.K.; Jacoeb, A.M.; Listiana, D., 2021. Fish oil extraction as a by-product of Tilapia (Oreochromis sp.) fish processing with dry rendering method. In: IOP Conference Series: Earth and Environmental Science. IOP Publishing, v. 679 (1), 012009. http://doi.org/ 10.1088/1755-1315/679/1/012009.

Tadros, T.F. (Ed.). Colloids and Interface Science Series. Wiley-VCH-Verlag, 2006.

Vaishnav, A.; Lal, J.; Mehta, N.K.; Mohanty, S.; Yadav, K.K.; Priyadarshini, M.B.; Debbarma, P.; Singh, N.S.; Pai, K.K. Singh, S.K., 2025. Unlocking the potential of fishery waste: exploring diverse applications of fish protein hydrolysates in food and nonfood sectors. Environmental Science and Pollution Research, 1-45. https://doi.org/10.1007/s11356-025-36244-3.

Valenzuela‐Ávila, L.; Miliar, Y.; Moya‐Ramírez, I.; Chyhyrynets, O.; García‐Román, M.; Altmajer‐Vaz, D., 2020. Effect of emulsification and hydrolysis pretreatments of waste frying oil on surfactin production. Journal of Chemical Technology Biotechnology, v. 95 (1), 223-231. https://doi.org/10.1002/jctb.6225

Villamil, O.; Váquiro, H.; Solanilla, J.F., 2017. Fish viscera protein hydrolysates: Production, potential applications and functional and bioactive properties. Food Chemistry, v. 224, 160-171. https://doi.org/10.1016/j.foodchem.2016.12.057

Wang, K.W.; Chen, J.X.; Liu, Q.Q.; Deng, X.; Luo, L.; Lin, S.M.; Chen, Y.J., 2022. A comparison between high carbohydrate and high lipid diets reception on the growth, feed utilization and glucose homeostasis of genetically improved farmed tilapia Oreochromis niloticus. Aquaculture Reports, v. 24, 101119. https://doi.org/10.1016/j.aqrep.2022.101119.

Yang, Y.; Gupta, V.K.; Du, Y.; Aghbashlo, M.; Show, P.L.; Pan, J.; Tabatabaei, M.; Rajaei, A., 2023. Potential application of polysaccharide mucilages as a substitute for emulsifiers: a review. International Journal of Biological Macromolecules, v. 242, 124800. https://doi.org/10.1016/j.ijbiomac.2023.124800.

Zhang, L.; Wu, H.X.; Li, W.J.; Qiao, F.; Zhang, W.B.; Du, Z.Y.; Zhang, M.L., 2023. Partial replacement of soybean meal by yellow mealworm (Tenebrio molitor) meal influences the flesh quality of Nile tilapia (Oreochromis niloticus). Animal Nutrition, v. 12, 108-115. https://doi.org/10.1016/j.aninu.2022.09.007.