Abstract
Objectives
When citrate and pyruvate were utilized to strengthen ATP generation for high cAMP production, oxidative stress became more severe in cells resulting in lower cell viability and cAMP formation at the late fermentation phase. To further improve cAMP biosynthesis, the effects of polyphosphate on cAMP fermentation performance together with intracellular ATP and oxidation levels were investigated under high oxidative stress condition and then high efficient cAMP fermentation process based on polyphosphate and salvage synthesis was developed and studied.
Results
With 2 g/L-broth sodium hexametaphosphate added at 24 h was determined as the optimal condition for cAMP production by Arthrobacter sp. CCTCC 2013431 in shake flasks. Under high oxidative stress condition caused by adding 15 mg/L-broth menadione, cAMP contents and cell viability were improved greatly due to hexametaphosphate addition and also exceeded those of control (without hexametaphosphate and menadione added) when fermentations were conducted in a 7 L bioreactor. Meanwhile, ATP levels and antioxidant capacity were improved obviously by hexametaphosphate as well. Moreover, a fermentation process with hexametaphosphate and hypoxanthine coupling added was developed by which cAMP concentration reached 7.25 g/L with an increment of 87.1% when compared with only hypoxanthine added batch and the high ROS contents generated from salvage synthesis were reduced significantly.
Conclusion
Polyphosphate could improve intracellular ATP levels and antioxidant capacity significantly under high oxidative stress condition resulting in enhanced cell viability and cAMP fermentation production no matter by de novo synthesis or salvage synthesis.
Similar content being viewed by others
References
Emanuel SL, Devaki B, Arthur RG et al (2020) Polyphosphate: a multifunctional metabolite in cyanobacteria and algae. Front Plant Sci 11:938. https://doi.org/10.3389/fpls.2020.00938
Li S, Ji J, Hu S et al (2020) Enhancement of ε-poly-L-lysine production in Streptomyces griseofuscus by addition of exogenous astaxanthin. Bioproc Biosyst Eng 43(10):1813–1821
Li Z, Chen B, Fang Z et al (2018) A novel fermentation process for cyclic adenosine monophosphate production based on citrate coupling hypoxanthine addition in pulses. Food Ferment Ind 44(11):154–158
Li Z, Chen B, Gu Y et al (2021a) Enhanced endogenous amino acids and energy metabolism level for cAMP biosynthesis by Arthrobacter sp. CCTCC 2013431 with citrate as cosubstrate. Biotechnol Lett. https://doi.org/10.1007/s10529-021-03170-6
Li Z, Zhang C, Tan H et al (2021b) Enhancing cAMP fermentation formation via glutathione and auxiliary energy substance coupling addition. Sci Technol Food Ind. https://doi.org/10.13386/j.issn1002-0306.2021010246
Liu Q, Wu C, Huang S et al (2018) Decreased hyperpolarization-activated cyclic nucleotide-gated channels are involved in bladder dysfunction associated with spinal cord injury. Int J Mol Med 41(5):2609–2618
Maureen CT, Marisol Z, Anton G et al (2019) Malaria inflammation by xanthine oxidase-produced reactive oxygen species. EMBO Mol Med 11:e9903. https://doi.org/10.15252/emmm.201809903
Niu HQ, Wang JZ, Zhuang W et al (2018) Comparative transcriptomic and proteomic analysis of Arthrobacter sp CGMCC 3584 responding to dissolved oxygen for cAMP production. Sci Rep 8(1):1–13
Niu HQ, Sun XZ, Song JR et al (2020) Knockout of pde gene in Arthrobacter sp. CGMCC 3584 and transcriptomic analysis of its effects on cAMP production. Bioproc Biosyst Eng 43(5):839–850
Resnick SM, Zehnder AJ (2000) In vitro ATP regeneration from polyphosphate and AMP by polyphosphate:AMP phosphotransferase and adenylate kinase from Acinetobacter johnsonii 210A. Appl Environ Microb 66(5):2045–2051
Shao HH, Tu YY, Wang YJ et al (2019) Oxidative stress response of Aspergillus oryzae induced by hydrogen peroxide and menadione sodium bisulfite. Microorganisms 7(8):225–237
Tabassum N, Kheya IS, Ibn SA et al (2020) A review on the possible leakage of electrons through the electron transport chain within mitochondria. J Biomed Res Environ Sci 6:105–113
Tang-Fichaux M, Chagneau CV, Bossuet-Greif N et al (2020) The polyphosphate kinase of Escherichia coli is required for full production of the genotoxin colibactin. mSphere 5:e01195-e1220. https://doi.org/10.1128/mSphere.01195-20
Xiao Q, Niu JR, Liu H et al (2019) High conversion of D-fructose into D-allulose by enzymes coupling with an ATP regeneration system. Mol Biotechnol 61:432–441
Yan P, Sun HB, Lu PQ et al (2018) Enhancement of ε-poly-L-lysine synthesis in Streptomyces by exogenous glutathione. Bioprocess Biosyst Eng 41:129–134
Yu L, Wu J, Liu J et al (2011) Enhanced curdlan production in Agrobacterium sp. ATCC 31749 by addition of low-polyphosphates. Biotechnol Bioproc E 16:34–41
Zeng X, Chen XS, Gao Y et al (2015) Continuously high reactive oxygen species generation decreased the specific ε-poly-L-lysine formation rate in fed-batch fermentation using glucose and glycerol as a mixed carbon source. Process Biochem 50(12):1993–2003
Funding
This work was financially supported by the Doctoral Scientific Research Foundation of Henan institute of science and technology (2015006).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, Z., Tan, H., Lu, N. et al. Enhanced ATP and antioxidant levels for cAMP biosynthesis by Arthrobacter sp. CCTCC 2013431 with polyphosphate addition. Biotechnol Lett 43, 2223–2231 (2021). https://doi.org/10.1007/s10529-021-03197-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-021-03197-9