Valorization of Bovine Manure and Molasses by the Production of Lactic Acid and Biomass through Probiotic Anaerobic Cofermentation with Lactobacillus acidophilus, Lactobacillus fermentum, and Bacillus subtilis
Publication: Journal of Environmental Engineering
Volume 150, Issue 2
Abstract
Lactic acid (LA) and probiotic biomass production were evaluated from bovine manure supported with 12% v/v molasses using three probiotic bacteria, Lactobacillus acidophilus, Lactobacillus fermentum, and Bacillus subtilis, with three inoculum concentrations, 5%, 10%, and 15% v/v. Laboratory-scale tests were carried out in 250-mL flasks (useful volume of 200 mL) at 37°C and 120 rpm for 72 h. During this time, samples were taken every 4 h to determine (1) the LA content using titration, (2) cell growth using the poured plate method, and (3) consumption of carbohydrates using the anthrone-sulfuric method. The data obtained were adjusted to the Gompertz generalized four-parameter model to obtain the kinetic parameters of the growth of the bacteria in the residue. With the species L. acidophilus at 10% v/v, the highest LA production yield was obtained, carbohydrates, with a concentration of () and values of and . With the same bacteria at 15% v/v, the biomass obtained had the highest concentration of proteins, 32.19% dry weight of proteins (). The results showed that bovine manure has the potential to produce LA and biomass, which are products with high nutritional, economic, and energetic value.
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Data Availability Statement
All data, models, and code generated or used during the study appear in the published paper.
Acknowledgments
The authors are grateful for the support for the infrastructure use facilities of the Tecnológico Nacional de México Campus Orizaba. Romero-Mota, Estrada-García, and Sales-Pérez thank the Consejo Nacional de Humanidades, Ciencias y Tecnologias (CONAHCYT) for the scholarship awarded for a Ph.D. degree with CVUs (scholarship holders) 608912, 1006558, and 1077313, respectively. This research was supported by the Tecnológico Nacional de México (TecNM) through Project 17205.23-P.
Author contributions: Conceptualization: J.M.M.C; methodology: D.I.R.M and J.E.G; validation: D.I.R.M and J.E.G.; formal analysis: D.I.R.M, J.e.g., R.E.S.P., and J.M.M.C.; investigation: D.I.R.M and J.E.G.; resources: J.M.M.C; writing—original draft preparation: D.I.R.M, J.e.g., R.E.S.P., and J.M.M.C.; writing—review and editing: D.I.R.M., J.e.g., R.E.S.P., and J.M.M.C.; supervision: J.M.M.C. All authors have read and agreed to the published version of the manuscript.
References
AGRICULTURA. 2022. Servicio de Información Agroalimentaria y Pesquera (SIAP). Mexico City, Mexico: Secretaria de Agricultura y Desarrollo Rural.
Aguirre-Ezkauriatza, E. J., A. Ramirez-Medrano, J. M. Aguilar-Yáñez, and M. M. Alvarez. 2009. “Producción de proteína y biomasa probiótica de Lactobacillus casei liofilizadas a partir de suero de leche de cabra.” Rev. Mex. Ing. Quim. 8 (1): 67–76.
APHA (American Public Health Association). 2017. Standard methods for the examination of water and wastewater. 23rd ed. 2–66. Washington, DC: APHA.
Aristimuño Ficoseco, C., F. I. Mansilla, G. M. Vignolo, and M. E. F. Nader-Macías. 2023. “Optimization of probiotic lactobacilli production for in-feed supplementation to feedlot cattle.” Appl. Microbiol. 3 (2): 339–357. https://doi.org/10.3390/applmicrobiol3020024.
Beegum, F. 2019. “Inhibitory effect of metabolites of Lactobacillus fermentum MH782089 grown in sucrose and dipotassium hydrogen phosphate supplemented paneer whey against Staphylococcus auereus.” Assessment 8 (12): 5.
Caulier, S., C. Nannan, A. Gillis, F. Licciardi, C. Bragard, and J. Mahillon. 2019. “Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis group.” Front. Microbiol. 10 (Feb): 302. https://doi.org/10.3389/fmicb.2019.00302.
Chen, B., Z. Su, K. Wang, B. Wang, Y. Wang, Z. Si, Y. Wu, D. Cai, and P. Qin. 2020. “Efficient lactic acid production from cassava bagasse by mixed culture of Bacillus coagulans and Lactobacillus rhamnosus using stepwise pH controlled simultaneous saccharification and co-fermentation.” Ind. Crops Prod. 146 (Apr): 112175. https://doi.org/10.1016/j.indcrop.2020.112175.
de Morais, A. M. M., B. R. A. Alencar, N. P. Leite, A. L. B. Firmo, E. D. Dutra, E. V. S. B. Sampaio, and R. S. C. Menezes. 2020. “Biogas production from co-digestion of different proportions of food waste and fresh bovine manure.” Biomass Convers. Biorefin. 12 (Jun): 2697–2704. https://doi.org/10.1007/s13399-020-00833-8.
Diario Oficial de la Federación. 2002. Protección ambiental: Lodos y biosólidos—Especificaciones y límites máximos permisibles de contaminantes para su aprovechamiento y disposición final. México: Diario Oficial de la Federación.
Estrada-García, J., E. Hernández-Aguilar, D. I. Romero-Mota, and J. M. Méndez-Contreras. 2023. “Influence of anaerobic biotransformation process of agro-industrial waste with Lactobacillus acidophilus on the rheological parameters: Case of study of pig manure.” Arch. Microbiol. 205 (3): 99. https://doi.org/10.1007/s00203-023-03437-8.
Gotz, L. F., A. Castamann, F. Piovesan, B. L. Anzolin, T. A. Herek, M. Mikoanski, and Y. L. Rita. 2019. “Use of rock powder associated with bovine manure in Latossolo Vermelho cultivated with wheat.” Rev. Bras. Agropecu. Sustentável 9 (2): 131–139.
Ince, O., Ç. Akyol, E. G. Ozbayram, B. Tutal, and B. Ince. 2020a. “Enhancing methane production from anaerobic co-digestion of cow manure and barley: Link between process parameters and microbial community dynamics.” Environ. Prog. Sustainable Energy 39 (1): 13292. https://doi.org/10.1002/ep.13292.
Ince, O., E. G. Ozbayram, Ç. Akyol, E. I. Erdem, G. Gunel, and B. Ince. 2020b. “Bacterial succession in the thermophilic phase of composting of anaerobic digestates.” Waste Biomass Valorization 11 (Mar): 841–849. https://doi.org/10.1007/s12649-018-0531-3.
Izaguirre, J. K., T. Dietrich, M. C. Villarán, and S. Castañón. 2020. “Protein hydrolysate from organic fraction of municipal solid waste compost as nitrogen source to produce lactic acid by Lactobacillus fermentum ATCC 9338 and Lactobacillus plantarum NCIMB 8823.” Process Biochem. 88 (Jan): 15–21. https://doi.org/10.1016/j.procbio.2019.09.028.
Jaffar, N. S., R. J. Jawan, and K. P. Chong. 2023. “The potential of lactic acid bacteria in mediating the control of plant diseases and plant growth stimulation in crop production—A mini review.” Front. Plant Sci. 13 (Jan): 1047945. https://doi.org/10.3389/fpls.2022.1047945.
Jeong, D.-E., Y. So, S.-Y. Park, S.-H. Park, and S.-H. Choi. 2018. “Random knock-in expression system for high yield production of heterologous protein in Bacillus subtilis.” J. Biotechnol. 266 (Jan): 50–58. https://doi.org/10.1016/j.jbiotec.2017.12.007.
Kumar, A., and S. R. Samadder. 2020. “Performance evaluation of anaerobic digestion technology for energy recovery from organic fraction of municipal solid waste: A review.” Energy 197 (Apr): 117253. https://doi.org/10.1016/j.energy.2020.117253.
Le, T. A. N., J. L. L. Lee, and W. N. Chen. 2023. “Stimulation of lactic acid production and Lactobacillus plantarum growth in the coculture with Bacillus subtilis using jackfruit seed starch.” J. Funct. Foods 104 (May): 105535. https://doi.org/10.1016/j.jff.2023.105535.
Lee, T.-Y., Y.-S. Lee, R.-H. Yeh, K.-H. Chen, and K.-L. Chen. 2022. “Bacillus amyloliquefaciens CU33 fermented feather meal-soybean meal product improves the intestinal morphology to promote the growth performance of broilers.” Poult. Sci. 101 (9): 102027. https://doi.org/10.1016/j.psj.2022.102027.
Li, S., S. Tang, Q. He, J. Gong, and J. Hu. 2019. “Physicochemical, textural and volatile characteristics of fermented milk co-cultured with Streptococcus thermophilus, Bifidobacterium animalis or Lactobacillus plantarum.” Int. J. Food Sci. Technol. 55 (2): 461–474. https://doi.org/10.1111/ijfs.14279.
López-Legarda, X., A. Taramuel-Gallardo, C. Arboleda-Echavarría, F. Segura-Sánchez, and L. Restrepo-Betancur. 2017. “Comparación de métodos que utilizan ácido sulfúrico para la determinación de azúcares totales.” Rev. Cub. Quím. 29 (2): 180–198.
Mæhre, H. K., L. Dalheim, G. K. Edvinsen, E. O. Elvevoll, and I.-J. Jensen. 2018. “Protein determination—Method matters.” Foods 7 (1): 5. https://doi.org/10.3390/foods7010005.
Mazguene, S. 2023. “Lactic acid bacteria metabolism: Mini-review.” Curr. Nutr. Food Sci. 19 (2): 94–104. https://doi.org/10.2174/1573401318666220527124256.
Mexican Standard. 2015. “Sistema Producto Leche–Alimentos–Lácteos– Determinación de acidez en leche fluida – Métodos de prueba.” Accessed April 6, 2015. https://vlex.com.mx/vid/declaratoria-vigencia-normas-mexicanas-563689866.
Mutungwazi, A., A. Awosusi, and T. S. Matambo. 2023. “Comparative functional microbiome profiling of various animal manures during their anaerobic digestion in biogas production processes.” Biomass Bioenergy 170 (Mar): 106728. https://doi.org/10.1016/j.biombioe.2023.106728.
Naghmouchi, K., Y. Belguesmia, F. Bendali, G. Spano, B. S. Seal, and D. Drider. 2020. “Lactobacillus fermentum: A bacterial species with potential for food preservation and biomedical applications.” Crit. Rev. Food Sci. Nutr. 60 (20): 3387–3399. https://doi.org/10.1080/10408398.2019.1688250.
Nehra, M., and S. Jain. 2023. “Estimation of renewable biogas energy potential from livestock manure: A case study of India.” Bioresour. Technol. Rep. 22 (Jun): 101432. https://doi.org/10.1016/j.biteb.2023.101432.
Niu, K., C. Chao, X. Zhang, Z. An, J. Zhou, and L. Yang. 2022. “Effects of different microbial agents on bedding treatment of ectopic fermentation of buffalo manure.” Front. Microbiol. 13 (Dec): 1080650. https://doi.org/10.3389/fmicb.2022.1080650.
Pasalari, H., M. Gholami, A. Rezaee, A. Esrafili, and M. Farzadkia. 2021. “Perspectives on microbial community in anaerobic digestion with emphasis on environmental parameters: A systematic review.” Chemosphere 270 (May): 128618. https://doi.org/10.1016/j.chemosphere.2020.128618.
Qin, S., S. Wainaina, H. Liu, A. M. Soufiani, A. Pandey, Z. Zhang, M. K. Awasthi, and M. J. Taherzadeh. 2021. “Microbial dynamics during anaerobic digestion of sewage sludge combined with food waste at high organic loading rates in immersed membrane bioreactors.” Fuel 303 (Nov): 121276. https://doi.org/10.1016/j.fuel.2021.121276.
Remes-Troche, M. J., et al. 2020. “Lactobacillus acidophilus LB: A useful pharmabiotic for the treatment of digestive disorders.” Ther. Adv. Gastroenterol. 13 (Nov): 1–15. https://doi.org/10.1177/1756284820971201.
Rogeri, R. C., L. T. Fuess, F. Eng, A. do Vale Borges, M. N. de Araujo, M. H. R. Z. Damianovic, and A. J. da Silva. 2023. “Strategies to control pH in the dark fermentation of sugarcane vinasse: Impacts on sulfate reduction, biohydrogen production and metabolite distribution.” J. Environ. Manage. 325 (Jan): 116495. https://doi.org/10.1016/j.jenvman.2022.116495.
Romero-Mota, D. I., J. Estrada-García, A. Alvarado-Lassman, and J. M. Méndez-Contreras. 2023. “Growth kinetics of Lactobacillus acidophilus during the anaerobic biotransformation process of agro-sugarcane waste.” Waste Biomass Valorization 14 (Mar): 3857–3867. https://doi.org/10.1007/s12649-023-02100-z.
Rosales-Bravo, H., J. Vázquez-Martínez, H. C. Morales-Torres, and V. Olalde-Portugal. 2020. “Evaluación de propiedades tecno-funcionales de cepas probióticas comerciales del género Lactobacillus.” Rev. Int. Investigación Innovación Tecnológica 8 (45): 1–19.
Sánchez-Valeriano, N., D. I. Romero-Mota, E. S. Rosas-Mendoza, E. Hernández-Aguilar, and J. M. Méndez-Contreras. 2022. “Determination of kinetic parameters of the anaerobic biotransformation process of corn cob (Zea mays L.) with Lactobacillus acidophilus.” Renewable Energy Biomass Sustainability 4 (1): 38–43. https://doi.org/10.56845/rebs.v4i1.67.
Senés-Guerrero, C., F. A. Colón-Contreras, J. F. Reynoso-Lobo, B. Tinoco-Pérez, J. H. Siller-Cepeda, and A. Pacheco. 2019. “Biogas-producing microbial composition of an anaerobic digester and associated bovine residues.” MicrobiologyOpen 8 (9): e00854. https://doi.org/10.1002/mbo3.854.
Solval, K. M., A. Chouljenko, A. Chotiko, and S. Sathivel. 2019. “Growth kinetics and lactic acid production of Lactobacillus plantarum NRRL B-4496, L. acidophilus NRRL B-4495, and L. reuteri B-14171 in media containing egg white hydrolysates.” LWT 105 (May): 393–399. https://doi.org/10.1016/j.lwt.2019.01.058.
Su, Y., C. Liu, H. Fang, and D. Zhang. 2020. “Bacillus subtilis: A universal cell factory for industry, agriculture, biomaterials and medicine.” Microb. Cell Fact. 19 (1): 1–12. https://doi.org/10.1186/s12934-020-01436-8.
Tata, P., C. Lue-Hing, J. J Bertucci, S. J. Sedita, and G. J. Knafl. 2000. “Class A biosolids production by a low-cost conventional technology.” Water Environ. Res. 72 (4): 413–422. https://doi.org/10.2175/106143000X137941.
Wang, K., M. Niu, D. Yao, J. Zhao, Y. Wu, B. Lu, and X. Zheng. 2019. “Physicochemical characteristics and in vitro and in vivo antioxidant activity of a cell-bound exopolysaccharide produced by Lactobacillus fermentum S1.” Int. J. Biol. Macromol. 139 (Oct): 252–261. https://doi.org/10.1016/j.ijbiomac.2019.07.200.
Wang, Y., J. Wu, M. Lv, Z. Shao, M. Hungwe, J. Wang, X. Bai, J. Xie, Y. Wang, and W. Geng. 2021. “Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry.” Front. Bioeng. Biotechnol. 9 (May): 612285. https://doi.org/10.3389/fbioe.2021.612285.
Yin, Y., Y. Hu, and J. Wang. 2022. “Co-fermentation of sewage sludge and lignocellulosic biomass for production of medium-chain fatty acids.” Bioresour. Technol. 361 (Oct): 127665. https://doi.org/10.1016/j.biortech.2022.127665.
Zetty-Arenas, A. M., L. P. Tovar, R. F. Alves, A. P. Mariano, W. van Gulik, R. Maciel Filho, and S. Freitas. 2021. “Co-fermentation of sugarcane bagasse hydrolysate and molasses by Clostridium saccharoperbutylacetonicum: Effect on sugar consumption and butanol production.” Ind. Crops Prod. 167 (Sep): 113512. https://doi.org/10.1016/j.indcrop.2021.113512.
Zhang, C., Y. Zhang, H. Li, and X. Liu. 2020. “The potential of proteins, hydrolysates and peptides as growth factors for Lactobacillus and Bifidobacterium: Current research and future perspectives.” Food Funct. 11 (3): 1946–1957. https://doi.org/10.1039/C9FO02961C.
Zhang, L., et al. 2022. “Complete genome analysis of Lactobacillus fermentum YLF016 and its probiotic characteristics.” Microb. Pathogen. 162 (Jan): 105212. https://doi.org/10.1016/j.micpath.2021.105212.
Zhang, L., X. T. Zhang, P. Jin, H. Zhao, X. Liu, and Q. Sheng. 2021. “Effects of oral administration of Spirulina platensis and probiotics on serum immunity indexes, colonic immune factors, fecal odor, and fecal flora in mice.” Anim. Sci. J. 92 (1): e13593. https://doi.org/10.1111/asj.13593.
Information & Authors
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Published In
Journal of Environmental Engineering
Volume 150 • Issue 2 • February 2024
Copyright
© 2023 American Society of Civil Engineers.
History
Received: Aug 15, 2023
Accepted: Sep 26, 2023
Published online: Nov 22, 2023
Published in print: Feb 1, 2024
Discussion open until: Apr 22, 2024
ASCE Technical Topics:
- Acids
- Agricultural wastes
- Bacteria
- Biological processes
- Biomass
- Chemical compounds
- Chemicals
- Chemistry
- Energy engineering
- Energy sources (by type)
- Engineering fundamentals
- Environmental engineering
- Fuels
- Laboratory tests
- Mathematics
- Non-renewable energy
- Parameters (statistics)
- Pollutants
- Renewable energy
- Statistics
- Tests (by type)
- Waste management
- Wastes
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