The role of lipids in fermentative propionate production from the co-fermentation of lipid and food waste

Abstract

● Lipid can promote PA production on a target from food waste.

● PA productivity reached 6.23 g/(L∙d) from co-fermentation of lipid and food waste.

● Lipid promoted the hydrolysis and utilization of protein in food waste.

● Prevotella , Veillonella and norank _f _Propioni bacteriaceae were enriched.

● Main pathway of PA production was the succinate pathway.

Food waste (FW) is a promising renewable low-cost biomass substrate for enhancing the economic feasibility of fermentative propionate production. Although lipids, a common component of food waste, can be used as a carbon source to enhance the production of volatile fatty acids (VFAs) during co-fermentation, few studies have evaluated the potential for directional propionate production from the co-fermentation of lipids and FW. In this study, co-fermentation experiments were conducted using different combinations of lipids and FW for VFA production. The contributions of lipids and FW to propionate production, hydrolysis of substrates, and microbial composition during co-fermentation were evaluated. The results revealed that lipids shifted the fermentation type of FW from butyric to propionic acid fermentation. Based on the estimated propionate production kinetic parameters, the maximum propionate productivity increased significantly with an increase in lipid content, reaching 6.23 g propionate/(L∙d) at a lipid content of 50%. Propionate-producing bacteria Prevotella, Veillonella, and norank_f_Propionibacteriaceae were enriched in the presence of lipids, and the succinate pathway was identified as a prominent fermentation route for propionate production. Moreover, the Kyoto Encyclopedia of Genes and Genomes functional annotation revealed that the expression of functional genes associated with amino acid metabolism was enhanced by the presence of lipids. Collectively, these findings will contribute to gaining a better understanding of targeted propionate production from FW.

Graphical abstract

Keywords

Acidogenic fermentation / Microbial community / Volatile fatty acid / Propionate / Food waste / Lipid

References

[1] AmmarE MPhilippidis G P (2021). Fermentative production of propionic acid: prospects and limitations of microorganisms and substrates. Applied Microbiology and Biotechnology, 105(16–17): 6199–6213

[2] Atasoy M, Eyice O, Schnurer A, Cetecioglu Z. (2019). Volatile fatty acids production via mixed culture fermentation: revealing the link between pH, inoculum type and bacterial composition. Bioresource Technology, 292: 121889

[3] Bevilacqua R, Regueira A, Mauricio-Iglesias M, Lema J M, Carballa M. (2021). Steering the conversion of protein residues to volatile fatty acids by adjusting pH. Bioresource Technology, 320: 124315

[4] Bose R S, Zakaria B S, Dhar B R, Tiwari M K. (2022). Effect of salinity and surfactant on volatile fatty acids production from kitchen wastewater fermentation. Bioresource Technology Reports, 18: 101017

[5] Chen Y, Randall A A, Mccue T. (2004). The efficiency of enhanced biological phosphorus removal from real wastewater affected by different ratios of acetic to propionic acid. Water Research, 38(1): 27–36

[6] Chowdhury B, Lin L, Dhar B R, Islam M N, Mccartney D, Kumar A. (2019). Enhanced biomethane recovery from fat, oil, and grease through co-digestion with food waste and addition of conductive materials. Chemosphere, 236: 124362

[7] CoralJKarp S GPorto De Souza Vandenberghe LParadaJ LPandeyASoccolC R (2008). Batch fermentation model of propionic acid production by Propionibacterium acidipropionici in different carbon sources. Applied Biochemistry and Biotechnology, 151(2–3): 333–341

[8] Costa-Gutierrez S B, Saez J M, Aparicio J D, Raimondo E E, Benimeli C S, Polti M A. (2021). Glycerol as a substrate for actinobacteria of biotechnological interest: advantages and perspectives in circular economy systems. Chemosphere, 279: 130505

[9] den Besten G, Van Eunen K, Groen A K, Venema K, Reijngoud D J, Bakker B M. (2013). The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research, 54(9): 2325–2340

[10] Elsamadony M, Mostafa A, Fujii M, Tawfik A, Pant D. (2021). Advances towards understanding long chain fatty acids-induced inhibition and overcoming strategies for efficient anaerobic digestion process. Water Research, 190: 116732

[11] Eş I, Khaneghah A M, Hashemi S M B, Koubaa M. (2017). Current advances in biological production of propionic acid. Biotechnology Letters, 39(5): 635–645

[12] Feng X, Ding Y, Xian M, Xu X, Zhang R, Zhao G. (2014). Production of optically pure d-lactate from glycerol by engineered Klebsiella pneumoniae strain. Bioresource Technology, 172: 269–275

[13] Garcia-AguirreJAymerichEGonzalez-Mtnez de Goñi JEsteban-Gutierrez M (2017). Selective VFA production potential from organic waste streams: assessing temperature and pH influence. Bioresource Technology, 244(Pt 1): 1081–1088

[14] Gonzalez-Garcia R, Mccubbin T, Navone L, Stowers C, Nielsen L, Marcellin E. (2017). Microbial propionic acid production. Fermentation (Basel, Switzerland), 3(2): 21

[15] He X, Yin J, Liu J, Chen T, Shen D. (2019). Characteristics of acidogenic fermentation for volatile fatty acid production from food waste at high concentrations of NaCl. Bioresource Technology, 271: 244–250

[16] Huang L, Chen Z, Xiong D, Wen Q, Ji Y. (2018). Oriented acidification of wasted activated sludge (WAS) focused on odd-carbon volatile fatty acid (VFA): regulation strategy and microbial community dynamics. Water Research, 142: 256–266

[17] Jiang J, Zhang Y, Li K, Wang Q, Gong C, Li M. (2013). Volatile fatty acids production from food waste: effects of pH, temperature, and organic loading rate. Bioresource Technology, 143: 525–530

[18] Jin C, Sun S, Yang D, Sheng W, Ma Y, He W, Li G. (2021). Anaerobic digestion: an alternative resource treatment option for food waste in China. Science of the Total Environment, 779: 146397

[19] Lalman J A, Komjarova I. (2004). Impact of long chain fatty acids on glucose fermentation under mesophilic conditions. Environmental Technology, 25(4): 391–401

[20] Lewis V P, Yang S T. (1992). Propionic acid fermentation by Propionibacterium acidipropionici: effect of growth substrate. Applied Microbiology and Biotechnology, 37(4): 437–442

[21] Li J, Zhang W, Li X, Ye T, Gan Y, Zhang A, Chen H, Xue G, Liu Y. (2018). Production of lactic acid from thermal pretreated food waste through the fermentation of waste activated sludge: effects of substrate and thermal pretreatment temperature. Bioresource Technology, 247: 890–896

[22] Li X, Chen Y, Zhao S, Wang D, Zheng X, Luo J. (2014). Lactic acid accumulation from sludge and food waste to improve the yield of propionic acid-enriched VFA. Biochemical Engineering Journal, 84: 28–35

[23] Liu N, Jiang J. (2020). Valorisation of food waste using salt to alleviate inhibition by animal fats and vegetable oils during anaerobic digestion. Biomass and Bioenergy, 143: 105826

[24] Liu N, Wang Q, Jiang J, Zhang H. (2017). Effects of salt and oil concentrations on volatile fatty acid generation in food waste fermentation. Renewable Energy, 113: 1523–1528

[25] Luo J, Fang S, Huang W, Wang F, Zhang L, Fang F, Cao J, Wu Y, Wang D. (2022). New insights into different surfactants’ impacts on sludge fermentation: focusing on the particular metabolic processes and microbial genetic traits. Frontiers of Environmental Science & Engineering, 16(8): 106

[26] Mazumdar S, Clomburg J M, Gonzalez R. (2010). Escherichia coli strains engineered for homofermentative production of D-lactic acid from glycerol. Applied and Environmental Microbiology, 76(13): 4327–4336

[27] Neves L, Oliveira R, Alves M M. (2009). Co-digestion of cow manure, food waste and intermittent input of fat. Bioresource Technology, 100(6): 1957–1962

[28] Ning Z, Zhang H, Li W, Zhang R, Liu G, Chen C. (2018). Anaerobic digestion of lipid-rich swine slaughterhouse waste: methane production performance, long-chain fatty acids profile and predominant microorganisms. Bioresource Technology, 269: 426–433

[29] Patel A, Sarkar O, Rova U, Christakopoulos P, Matsakas L. (2021). Valorization of volatile fatty acids derived from low-cost organic waste for lipogenesis in oleaginous microorganisms: a review. Bioresource Technology, 321: 124457

[30] Ranaei V, Pilevar Z, Mousavi Khaneghah A, Hosseini H. (2020). Propionic acid: method of production, current state and perspectives. Food Technology and Biotechnology, 58(2): 115–127

[31] Rombouts J L, Kranendonk E M M, Regueira A, Weissbrodt D G, Kleerebezem R, Loosdrecht M C M. (2020). Selecting for lactic acid producing and utilising bacteria in anaerobic enrichment cultures. Biotechnology and Bioengineering, 117(5): 1281–1293

[32] Strobel H J. (1992). Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23. Applied and Environmental Microbiology, 58(7): 2331–2333

[33] Tan L C, Lin R, Murphy J D, Lens P N L. (2021). Granular activated carbon supplementation enhances anaerobic digestion of lipid-rich wastewaters. Renewable Energy, 171: 958–970

[34] Usman M, Zhao S, Jeon B H, Salama E S, Li X. (2022). Microbial beta-oxidation of synthetic long-chain fatty acids to improve lipid biomethanation. Water Research, 213: 118164

[35] Vidal-Antich C, Perez-Esteban N, Astals S, Peces M, Mata-Alvarez J, Dosta J. (2021). Assessing the potential of waste activated sludge and food waste co-fermentation for carboxylic acids production. Science of the Total Environment, 757: 143763

[36] Wang D, Ai J, Shen F, Yang G, Zhang Y, Deng S, Zhang J, Zeng Y, Song C. (2017). Improving anaerobic digestion of easy-acidification substrates by promoting buffering capacity using biochar derived from vermicompost. Bioresource Technology, 227: 286–296

[37] Xiao K, Yu Z, Pei K, Sun M, Zhu Y, Liang S, Hou H, Liu B, Hu J, Yang J. (2022). Anaerobic digestion of sludge by different pretreatments: changes of amino acids and microbial community. Frontiers of Environmental Science & Engineering, 16(2): 23

[38] XuYWangX LiZChengS JiangJ (2022). Potential of food waste hydrolysate as an alternative carbon source for microbial oil synthesis. Bioresource Technology, 344(Pt B): 126312

[39] Yin J, Liu J, Chen T, Long Y, Shen D. (2019). Influence of melanoidins on acidogenic fermentation of food waste to produce volatility fatty acids. Bioresource Technology, 284: 121–127

[40] Yin J, Yu X, Wang K, Shen D. (2016a). Acidogenic fermentation of the main substrates of food waste to produce volatile fatty acids. International Journal of Hydrogen Energy, 41(46): 21713–21720

[41] Yin J, Yu X, Zhang Y, Shen D, Wang M, Long Y, Chen T. (2016b). Enhancement of acidogenic fermentation for volatile fatty acid production from food waste: effect of redox potential and inoculum. Bioresource Technology, 216: 996–1003

[42] Zhang P, Chen Y, Zhou Q. (2009). Waste activated sludge hydrolysis and short-chain fatty acids accumulation under mesophilic and thermophilic conditions: effect of pH. Water Research, 43(15): 3735–3742

RIGHTS & PERMISSIONS

Higher Education Press