Abstract
Bio-based succinic acid production has attracted global attention since its consideration as a potential replacement to petroleum-based platform chemicals. This study used three different CO2 sources, namely NaHCO3, K2CO3 and MgCO3 for fermentation of succinic acid (SA) by Actinobacillus succinogenes under three distinct substrate conditions i.e. lactose, whey and whey devoid of any supplements. Batch experiments were performed in both anaerobic flasks and 5L benchtop fermenter. SA fermentation in anaerobic flasks was unfettered by supplementary nutrients. However, fermentation in the benchtop fermenter devoid of supplementary nutrients resulted into 42% reduction in SA yield as well as lower SA productivities. Furthermore, a significant reduction of cell growth occurred in anerobic flasks at pH < 6.0, and complete termination of bacterial activity was noted at pH < 5.3. The highest SA titer, yield and productivity of 15.67 g/L, 0.54 g/g and 0.33 g/L/h, respectively, was recorded from whey fermentation with MgCO3. The present study further highlights significant inhibitory effect of K2CO3 buffered medium on Actinobacillus succinogenes. Thus, we can claim that environmental pollution as well as costs of SA production from whey can be reduced by leveraging on whey residual nutrients to support the activity of Actinobacillus succinogenes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bozell JJ, Petersen GR (2010) Technology development for the production of biobased products from biorefinery carbohydrates—the US Department of Energy’s “Top 10” revisited. Green Chem 12:539–554. https://doi.org/10.1039/B922014C
Carvalho F, Prazeres AR, Rivas J (2013) Cheese whey wastewater: Characterization and treatment. Sci Total Environ 445–446:385–396. https://doi.org/10.1016/J.SCITOTENV.2012.12.038
Cimini D, Argenzio O, D’Ambrosio S et al (2016) Production of succinic acid from Basfia succiniciproducens up to the pilot scale from Arundo donax hydrolysate. Bioresour Technol 222:355–360. https://doi.org/10.1016/j.biortech.2016.10.004
Corona-González RI, Bories A, González-Álvarez V, Pelayo-Ortiz C (2008) Kinetic study of succinic acid production by Actinobacillus succinogenes ZT-130. Process Biochem 43:1047–1053. https://doi.org/10.1016/j.procbio.2008.05.011
Corona-González RI, Miramontes-Murillo R, Arriola-Guevara E et al (2014) Immobilization of Actinobacillus succinogenes by adhesion or entrapment for the production of succinic acid. Bioresour Technol 164:113–118. https://doi.org/10.1016/j.biortech.2014.04.081
Corona-Gonzalez RI, Bories A, González-Álvarez V et al (2010) Succinic acid production with Actinobacillus succinogenes ZT-130 in the presence of succinic acid. Curr Microbiol 60:71–77. https://doi.org/10.1007/s00284-009-9504-x
Guettler MV, Rumler D, Jain MK (1999) Actinobacillus succinogenes sp. nov., a novel succinic-acid-producing strain from the bovine 1umen. Int J Syst Bacteriol 49:207–216. https://doi.org/10.1099/00207713-49-1-207
Herselman J, Bradfield MFA, Vijayan U, Nicol W (2017) The effect of carbon dioxide availability on succinic acid production with biofilms of Actinobacillus succinogenes. Biochem Eng J 117:218–225. https://doi.org/10.1016/j.bej.2016.10.018
Huang M, Cheng J, Chen P et al (2019) Efficient production of succinic acid in engineered Escherichia coli strains controlled by anaerobically-induced nirB promoter using sweet potato waste hydrolysate. J Environ Manage 237:147–154. https://doi.org/10.1016/j.jenvman.2019.02.041
Jansen MLA, van Gulik WM (2014) Towards large scale fermentative production of succinic acid. Curr Opin Biotechnol 30:190–197. https://doi.org/10.1016/J.COPBIO.2014.07.003
Kim DY, Yim SC, Lee PC et al (2004) Batch and continuous fermentation of succinic acid from wood hydrolysate by Mannheimia succiniciproducens MBEL55E. Enzyme Microb Technol 35:648–653. https://doi.org/10.1016/J.ENZMICTEC.2004.08.018
Lee PC, Lee WG, Kwon S et al (2000) Batch and continuous cultivation of Anaerobiospirillum succiniciproducens for the production of succinic acid from whey. Appl Microbiol Biotechnol 54:23–27. https://doi.org/10.1007/s002530000331
Lee PC, Lee SY, Hong SH, Chang HN (2003) Batch and continuous cultures of Mannheimia succiniciproducens MBEL55E for the production of succinic acid from whey and corn steep liquor. Bioprocess Biosyst Eng 26:63–67. https://doi.org/10.1007/s00449-003-0341-1
Lin H, San KY, Bennett GN (2005) Effect of Sorghum vulgare phosphoenolpyruvate carboxylase and Lactococcus lactis pyruvate carboxylase coexpression on succinate production in mutant strains of Escherichia coli. Appl Microbiol Biotechnol 67:515–523. https://doi.org/10.1007/s00253-004-1789-x
Lin SKC, Du C, Koutinas A et al (2008) Substrate and product inhibition kinetics in succinic acid production by Actinobacillus succinogenes. Biochem Eng J 41:128–135. https://doi.org/10.1016/j.bej.2008.03.013
Liu YP, Zheng P, Sun ZH et al (2008a) Economical succinic acid production from cane molasses by Actinobacillus succinogenes. Bioresour Technol 99:1736–1742. https://doi.org/10.1016/j.biortech.2007.03.044
Liu YP, Zheng P, Sun ZH et al (2008b) Strategies of pH control and glucose-fed batch fermentation for production of succinic acid by Actinobacillus succinogenes CGMCC1593. J Chem Technol Biotechnol 83:722–729. https://doi.org/10.1002/jctb.1862
Longanesi L, Frascari D, Spagni C et al (2018) Succinic acid production from cheese whey by biofilms of Actinobacillus succinogenes: packed bed bioreactor tests. J Chem Technol Biotechnol 93:246–256. https://doi.org/10.1002/jctb.5347
Louasté B, Eloutassi N (2020) Succinic acid production from whey and lactose by Actinobacillus succinogenes 130Z in batch fermentation. Biotechnol Reports 27:e00481. https://doi.org/10.1016/j.btre.2020.e00481
McKinlay JB, Zeikus JG, Vieille C (2005) Insights into Actinobacillus succinogenes fermentative metabolism in a chemically defined growth medium. Appl Environ Microbiol 71:6651–6656. https://doi.org/10.1128/AEM.71.11.6651-6656.2005
McKinlay JB, Shachar-Hill Y, Zeikus JG, Vieille C (2007) Determining Actinobacillus succinogenes metabolic pathways and fluxes by NMR and GC-MS analyses of 13C-labeled metabolic product isotopomers. Metab Eng 9:177–192. https://doi.org/10.1016/j.ymben.2006.10.006
Olajuyin AM, Yang M, Liu Y et al (2016) Efficient production of succinic acid from Palmaria palmata hydrolysate by metabolically engineered Escherichia coli. Bioresour Technol 214:653–659. https://doi.org/10.1016/j.biortech.2016.04.117
Pateraki C, Patsalou M, Vlysidis A et al (2016) Actinobacillus succinogenes: Advances on succinic acid production and prospects for development of integrated biorefineries. Biochem Eng J 112:285–303. https://doi.org/10.1016/J.BEJ.2016.04.005
Rajendra U, Vijayan P, Nicol W (2016) Continuous production of succinic acid with Actinobacillus succinogenes biofilms: Effect of complex nitrogen source on yield and productivity
Saidi V, Sheikh-Zeinoddin M, Kobarfard F, SoleimanianZad S (2020) Bioactive characteristics of a semi-hard non-starter culture cheese made from raw or pasteurized sheep’s milk. 3 Biotech 10:85. https://doi.org/10.1007/s13205-020-2075-z
Salvachúa D, Mohagheghi A, Smith H et al (2016) Succinic acid production on xylose-enriched biorefinery streams by Actinobacillus succinogenes in batch fermentation. Biotechnol Biofuels 9:1–15. https://doi.org/10.1186/s13068-016-0425-1
Samuelov NS, Datta R, Jain MK, Zeikus JG (1999) Whey fermentation by Anaerobiospirillum succiniciproducens for production of a succinate-based animal feed additive. Appl Environ Microbiol 65:2260–2263. https://doi.org/10.1128/aem.65.5.2260-2263.1999
Shen N, Qin Y, Wang Q et al (2015) Production of succinic acid from sugarcane molasses supplemented with a mixture of corn steep liquor powder and peanut meal as nitrogen sources by Actinobacillus succinogenes. Lett Appl Microbiol 60:544–551. https://doi.org/10.1111/lam.12399
Shen N, Zhang H, Qin Y et al (2018) Efficient production of succinic acid from duckweed (Landoltia punctata) hydrolysate by Actinobacillus succinogenes GXAS137. Bioresour Technol 250:35–42. https://doi.org/10.1016/j.biortech.2017.09.208
Sorokina KN, Samoylova YV, Gromov NV et al (2020) Production of biodiesel and succinic acid from the biomass of the microalga Micractinium sp IC-44. Bioresour Technol. 317:124026. https://doi.org/10.1016/j.biortech.2020.124026
Van Der Werf MJ, Guettler MV, Jain MK, Zeikus JG (1997) Environmental and physiological factors affecting the succinate product ratio during carbohydrate fermentation by Actinobacillus sp. 130Z. Arch Microbiol 167:332–342. https://doi.org/10.1007/s002030050452
Wan C, Li Y, Shahbazi A, Xiu S (2008) Succinic acid production from cheese whey using Actinobacillus succinogenes 130 Z. Appl Biochem Biotechnol 145:111–119. https://doi.org/10.1007/s12010-007-8031-0
Wang D, Li Q, Song Z et al (2011) High cell density fermentation via a metabolically engineered Escherichia coli for the enhanced production of succinic acid. J Chem Technol Biotechnol 86:512–518. https://doi.org/10.1002/jctb.2543
Yadav JSS, Yan S, Pilli S et al (2015) Cheese whey: A potential resource to transform into bioprotein, functional/nutritional proteins and bioactive peptides. Biotechnol Adv 33:756–774
Yu J, Li Z, Ye Q et al (2010) Development of succinic acid production from corncob hydrolysate by Actinobacillus succinogenes. J Ind Microbiol Biotechnol. https://doi.org/10.1007/s10295-010-0750-5
Yu Q, Cui Z, Zheng Y et al (2018) Exploring succinic acid production by engineered Yarrowia lipolytica strains using glucose at low pH. Biochem Eng J 139:51–56. https://doi.org/10.1016/j.bej.2018.08.001
Zhang Y, Li Q, Zhang Y et al (2012) Optimization of succinic acid fermentation with Actinobacillus succinogenes by response surface methodology (RSM). J Zhejiang Univ Sci B 13:103–110. https://doi.org/10.1631/jzus.B1100134
Zheng P, Dong JJ, Sun ZH et al (2009) Fermentative production of succinic acid from straw hydrolysate by Actinobacillus succinogenes. Bioresour Technol 100:2425–2429. https://doi.org/10.1016/j.biortech.2008.11.043
Zhu LW, Wang CC, Liu RS et al (2012) Actinobacillus succinogenes ATCC 55618 fermentation medium optimization for the production of succinic acid by response surface methodology. J Biomed Biotechnol. https://doi.org/10.1155/2012/626137
Zou W, Zhu LW, Li HM, Tang YJ (2011) Significance of CO 2donor on the production of succinic acid by Actinobacillus succinogenes ATCC 55618. Microb Cell Fact 10:1–10. https://doi.org/10.1186/1475-2859-10-87
Acknowledgements
We wish to thank the Scientific and Technological Research Council of Turkey (TÜBITAK) for providing the financial support under project No. 115Y824
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflict of interest in the publication.
Rights and permissions
About this article
Cite this article
Omwene, P.I., Yağcıoğlu, M., Öcal-Sarihan, Z.B. et al. Batch fermentation of succinic acid from cheese whey by Actinobacillus succinogenes under variant medium composition. 3 Biotech 11, 389 (2021). https://doi.org/10.1007/s13205-021-02939-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-021-02939-w