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Heterotrophic nitrification and aerobic denitrification characteristics of the psychrotolerant Pseudomonas peli NR-5 at low temperatures

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Abstract

The nitrogen removal efficiency of heterotrophic nitrification and aerobic denitrification (HN–AD) bacteria can be seriously inhibited at low temperatures (< 15 °C). A novel psychrotolerant bacterium, Pseudomonas peli NR-5 (P. peli NR-5), with efficient HN–AD capability was isolated and screened from river sediments in cold areas. When P. peli NR-5 was aerobically cultivated for 60 h at 10 °C with NH4+-N, NO3−-N, and NO2−-N as the sole nitrogen sources (N 105 mg/L), the nitrogen removal efficiencies were 97.3, 95.3, and 87.8%, respectively, without nitrite accumulation, and the corresponding average nitrogen removal rates were 1.71, 1.67, and 1.55 mg/L/h, respectively. Meanwhile, P. peli NR-5 exhibited excellent simultaneous nitrification and denitrification capabilities at 10 °C. Sodium succinate was the most favorable carbon substrate for bacterial growth and ammonia removal by strain NR-5. The optimal culture conditions determined by the response surface methodology model were a carbon to nitrogen ratio of 5.9, temperature of 11.5 °C, pH of 7.0, and shaking speed of 144 rpm. Under these conditions, 99.1% of the total nitrogen was removed in the verification experiments, which was not significantly different from the predicted maximum removal in the model (99.6%). Six functional genes participating in the HN–AD process were successfully obtained by polymerase chain reaction amplification, which further confirmed the HN–AD capability of P. peli NR-5 and proposed the metabolic pathway of HN–AD. The above results provide a theoretical background of psychrotolerant HN–AD bacteria in wastewater purification under low-temperature conditions.

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The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Li Y, Zhang L, Liu W, Zhou Z (2022) Simultaneous removal of urea nitrogen and inorganic nitrogen from high-salinity wastewater by Halomonas sp. H36. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-022-22018-8

    Article  Google Scholar 

  2. Xiong J, Guo S, Hou Y, Dai Z, Zhu H, Wang S, Chen G (2019) Using the modified sugarcane bagasse cellulose cation membrane as a separator in the electrodialysis device for ammonia nitrogen removal. J Biobased Mater Bio 13:475–483. https://doi.org/10.1166/jbmb.2019.1875

    Article  CAS  Google Scholar 

  3. Song W, Li Z, Liu F, Ding Y, Qi P, You H, Jin C (2018) Effective removal of ammonia nitrogen from waste seawater using crystal seed enhanced struvite precipitation technology with response surface methodology for process optimization. Environ Sci Pollut Res 25:628–638. https://doi.org/10.1007/s11356-017-0441-0

    Article  CAS  Google Scholar 

  4. Hu Z, Liu J, Zheng W, Li D, Liu Y, Yao H (2019) Highly-efficient nitrogen removal from domestic wastewater based on enriched aerobic/anoxic biological filters and functional microbial community characteristics. J Clean Prod 238:117867. https://doi.org/10.1016/j.jclepro.2019.117867

    Article  CAS  Google Scholar 

  5. Zhang S, Sun X, Fan Y, Qiu T, Gao M, Wang X (2017) Heterotrophic nitrification and aerobic denitrification by Diaphorobacter polyhydroxybutyrativorans SL-205 using poly(3-hydroxybutyrate-co-3-hydroxyvalerate) as the sole carbon source. Bioresour Technol 241:500–507. https://doi.org/10.1016/j.biortech.2017.05.185

    Article  CAS  PubMed  Google Scholar 

  6. Ren J, Cheng X, Ma H, Ma X (2021) Characteristics of a novel heterotrophic nitrification and aerobic denitrification bacterium and its bioaugmentation performance in a membrane bioreactor. Bioresour Technol 342:125908. https://doi.org/10.1016/j.biortech.2021.125908

    Article  CAS  PubMed  Google Scholar 

  7. Angar Y, Kebbouche-Gana S, Djelali NE, Khemili-Talbi S (2016) Novel approach for the ammonium removal by simultaneous heterotrophic nitrification and denitrification using a novel bacterial species co-culture. World J Microb Biot 32:36–49. https://doi.org/10.1007/s11274-015-2007-y

    Article  CAS  Google Scholar 

  8. Yang M, Lu D, Yang J, Zhao Y, Zhao Q, Sun Y, Liu H, Ma J (2019) Carbon and nitrogen metabolic pathways and interaction of cold-resistant heterotrophic nitrifying bacteria under aerobic and anaerobic conditions. Chemosphere 234:162–170. https://doi.org/10.1016/j.chemosphere.2019.06.052

    Article  CAS  PubMed  Google Scholar 

  9. Xu Y, He T, Li Z, Ye Q, Chen Y, Xie E, Zhang X (2017) Nitrogen removal characteristics of Pseudomonas putida Y-9 capable of heterotrophic nitrification and aerobic denitrification at low temperature. BioMed Res Int 2017:1429018. https://doi.org/10.1155/2017/1429018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Robertson LA, Kuenen JG (1984) Aerobic denitrification: a controversy revived. Arch Microbio 139:351–354. https://doi.org/10.1007/BF00408378

    Article  CAS  Google Scholar 

  11. Zhang D, Li W, Huang X, Qin W, Liu M (2013) Removal of ammonium in surface water at low temperature by a newly isolated Microbacterium sp. strain SFA13. Bioresour Technol 137:147–152. https://doi.org/10.1016/j.biortech.2013.03.094

    Article  CAS  PubMed  Google Scholar 

  12. Liu Y, Wang Y, Li Y, An H, Lv Y (2015) Nitrogen removal characteristics of heterotrophic nitrification-aerobic denitrification by Alcaligenes faecalis C16. Chinese J Chem Eng 23:827–834. https://doi.org/10.1016/j.cjche.2014.04.005

    Article  CAS  Google Scholar 

  13. Wei R, Hui C, Zhang Y, Jiang H, Zhao Y, Du L (2021) Nitrogen removal characteristics and predicted conversion pathways of a heterotrophic nitrification-aerobic denitrification bacterium, Pseudomonas aeruginosa P-1. Enivrion Sci Pollut Res 28:7503–7514. https://doi.org/10.1007/s11356-020-11066-7

    Article  CAS  Google Scholar 

  14. Yang L, Ren YX, Liang X, Zhao SQ, Wang JP, Xia ZH (2015) Nitrogen removal characteristics of a heterotrophic nitrifier Acinetobacter junii YB and its potential application for the treatment of high-strength nitrogenous wastewater. Bioresour Technol 193:227–233. https://doi.org/10.1016/j.biortech.2015.05.075

    Article  CAS  PubMed  Google Scholar 

  15. Yang M, Lu D, Qin B, Liu Q, Zhao Y, Liu H, Ma J (2018) Highly efficient nitrogen removal of a coldness-resistant and low nutrient needed bacterium, Janthinobacterium sp. M-11. Bioresour Technol 256:366–373. https://doi.org/10.1016/j.biortech.2018.02.049

    Article  CAS  PubMed  Google Scholar 

  16. Ge Q, Yue X, Wang G (2015) Simultaneous heterotrophic nitrification and aerobic denitrification at high initial phenol concentration by isolated bacterium Diaphorobacter sp. PD-7. Chinese J Chem Eng 23:835–841. https://doi.org/10.1016/j.cjche.2015.02.001

    Article  CAS  Google Scholar 

  17. Ren YX, Yang L, Liang X (2014) The characteristics of a novel heterotrophic nitrifying and aerobic denitrifying bacterium, Acinetobacter junii YB. Bioresour Technol 171:1–9. https://doi.org/10.1016/j.biortech.2014.08.058

    Article  CAS  PubMed  Google Scholar 

  18. Qu J, Zhao R, Chen Y, Li Y, Jin P, Zheng Z (2022) Enhanced nitrogen removal from low-temperature wastewater by an iterative screening of cold-tolerant denitrifying bacteria. Bioproc Biosyst Eng 45:381–390. https://doi.org/10.1007/s00449-021-02668-7

    Article  CAS  Google Scholar 

  19. Xi H, Zhou X, Arslan M, Luo Z, Wei J, Wu Z, Gamal El-Din M (2022) Heterotrophic nitrification and aerobic denitrification process: promising but a long way to go in the wastewater treatment. Sci Total Environ 805:150212. https://doi.org/10.1016/j.scitotenv.2021.150212

    Article  CAS  PubMed  Google Scholar 

  20. He T, Xie D, Li Z, Ni J, Sun Q (2017) Ammonium stimulates nitrate reduction during simultaneous nitrification and denitrification process by Arthrobacter arilaitensis Y-10. Bioresour Technol 239:66–73. https://doi.org/10.1016/j.biortech.2017.04.125

    Article  CAS  PubMed  Google Scholar 

  21. Guo Y, Wang Y, Zhang Z, Huang F, Chen S (2018) Physiological and transcriptomic insights into the cold adaptation mechanism of a novel heterotrophic nitrifying and aerobic denitrifying-like bacterium Pseudomonas indoloxydans YY-1. Int Biodeter Biodegr 134:16–24. https://doi.org/10.1016/j.ibiod.2018.08.001

    Article  CAS  Google Scholar 

  22. Zhang X, Xia Y, Zeng Y, Sun X, Tao R, Mei Y, Qu M (2022) Simultaneous nitrification and denitrification by Pseudomonas sp. Y-5 in a high nitrogen environment. Environ Sci Pollut Res 29:69491–69501. https://doi.org/10.1007/s11356-022-20708-x

    Article  CAS  Google Scholar 

  23. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association (APHA), Washington, DC, USA

    Google Scholar 

  24. Xia L, Li X, Fan W, Wang J (2020) Heterotrophic nitrification and aerobic denitrification by a novel Acinetobacter sp. ND7 isolated from municipal activated sludge. Bioresour Technol 301:122749. https://doi.org/10.1016/j.biortech.2020.122749

    Article  CAS  PubMed  Google Scholar 

  25. Cui Y, Cui YW, Huang JL (2021) A novel halophilic Exiguobacterium mexicanum strain removes nitrogen from saline wastewater via heterotrophic nitrification and aerobic denitrification. Bioresour Technol 333:125189. https://doi.org/10.1016/j.biortech.2021.125189

    Article  CAS  PubMed  Google Scholar 

  26. Lei X, Jia Y, Chen Y, Hu Y (2019) Simultaneous nitrification and denitrification without nitrite accumulation by a novel isolated Ochrobactrum anthropic LJ81. Bioresour Technol 272:442–450. https://doi.org/10.1016/j.biortech.2018.10.060

    Article  CAS  PubMed  Google Scholar 

  27. Yang Q, Yang T, Shi Y, Xin Y, Zhang L, Gu Z, Li Y, Ding Z, Shi G (2021) The nitrogen removal characterization of a cold-adapted bacterium: Bacillus simplex H-b. Bioresour Technol 323:124554. https://doi.org/10.1016/j.biortech.2020.124554

    Article  CAS  PubMed  Google Scholar 

  28. Lang X, Li Q, Ji M, Yan G, Guo S (2020) Isolation and niche characteristics in simultaneous nitrification and denitrification application of an aerobic denitrifier, Acinetobacter sp. YS2. Bioresour Technol 302:122799. https://doi.org/10.1016/j.biortech.2020.122799

    Article  CAS  PubMed  Google Scholar 

  29. Jin R, Liu T, Liu G, Zhou J, Huang J, Wang A (2015) Simultaneous heterotrophic nitrification and aerobic denitrification by the marine origin bacterium Pseudomonas sp. ADN-42. Appl Biochem Biotech 175:2000–2011. https://doi.org/10.1007/s12010-014-1406-0

    Article  CAS  Google Scholar 

  30. Jin P, Chen Y, Yao R, Zheng Z, Du Q (2019) New insight into the nitrogen metabolism of simultaneous heterotrophic nitrification-aerobic denitrification bacterium in mRNA expression. J Hazard Mater 371:295–303. https://doi.org/10.1016/j.jhazmat.2019.03.023

    Article  CAS  PubMed  Google Scholar 

  31. Zhao B, Cheng DY, Tan P, An Q, Guo JS (2018) Characterization of an aerobic denitrifier Pseudomonas stutzeri strain XL-2 to achieve efficient nitrate removal. Bioresour Technol 250:564–573. https://doi.org/10.1016/j.biortech.2017.11.038

    Article  CAS  PubMed  Google Scholar 

  32. Yang T, Xin Y, Zhang L, Gu Z, Li Y, Ding Z, Shi G (2020) Characterization on the aerobic denitrification process of Bacillus strains. Biomass Bioenerg 140:105677. https://doi.org/10.1016/j.biombioe.2020.105677

    Article  CAS  Google Scholar 

  33. Ye Q, Li K, Li Z, Xu Y, He T, Tang W, Xiang S (2017) Heterotrophic nitrification-aerobic denitrification performance of Strain Y-12 under low temperature and high concentration of inorganic nitrogen conditions. Water 9:835. https://doi.org/10.3390/w9110835

    Article  CAS  Google Scholar 

  34. Ke X, Liu C, Tang SQ, Guo TT, Pan L, Xue YP, Zheng YG (2022) Characterization of Acinetobacter indicus ZJB20129 for heterotrophic nitrification and aerobic denitrification isolated from an urban sewage treatment plant. Bioresour Technol 347:126423. https://doi.org/10.1016/j.biortech.2021.126423

    Article  CAS  PubMed  Google Scholar 

  35. Chen S, He S, Wu C, Du D (2019) Characteristics of heterotrophic nitrification and aerobic denitrification bacterium Acinetobacter sp. T1 and its application for pig farm wastewater treatment. J Biosci Bioeng 127:201–205. https://doi.org/10.1016/j.jbiosc.2018.07.025

    Article  CAS  PubMed  Google Scholar 

  36. He T, Li Z, Sun Q, Xu Y, Ye Q (2016) Heterotrophic nitrification and aerobic denitrification by Pseudomonas tolaasii Y-11 without nitrite accumulation during nitrogen conversion. Bioresour Technol 200:493–499. https://doi.org/10.1016/j.biortech.2015.10.064

    Article  CAS  PubMed  Google Scholar 

  37. Zhao T, Chen P, Zhang L, Zhang L, Gao Y, Ai S, Liu H, Liu X (2021) Heterotrophic nitrification and aerobic denitrification by a novel Acinetobacter sp. TAC-1 at low temperature and high ammonia nitrogen. Bioresour Technol 339:125620. https://doi.org/10.1016/j.biortech.2021.125620

    Article  CAS  PubMed  Google Scholar 

  38. Lei Y, Wang Y, Liu H, Xi C, Song L (2016) A novel heterotrophic nitrifying and aerobic denitrifying bacterium, Zobellella taiwanensis DN-7, can remove high-strength ammonium. Appl Microbiol Biotechnol 100:4219–4229. https://doi.org/10.1007/s00253-016-7290-5

    Article  CAS  PubMed  Google Scholar 

  39. Chen H, Zhou W, Zhu S, Liu F, Qin L, Xu C, Wang Z (2021) Biological nitrogen and phosphorus removal by a phosphorus-accumulating bacteria Acinetobacter sp. strain C-13 with the ability of heterotrophic nitrification-aerobic denitrification. Bioresour Technol 322:124507. https://doi.org/10.1016/j.biortech.2020.124507

    Article  CAS  PubMed  Google Scholar 

  40. Huang F, Pan L, Lv N, Tang X (2017) Characterization of novel Bacillus strain N31 from mariculture water capable of halophilic heterotrophic nitrification-aerobic denitrification. J Biosci Bioeng 124:564–571. https://doi.org/10.1016/j.jbiosc.2017.06.008

    Article  CAS  PubMed  Google Scholar 

  41. Zheng Z, Zhang D, Li W, Qin W, Huang X, Lv L (2018) Substrates removal and growth kinetic characteristics of a heterotrophic nitrifying-aerobic denitrifying bacterium, Acinetobacter harbinensis HITLi7(T) at 2 degrees C. Bioresour Technol 259:286–293. https://doi.org/10.1016/j.biortech.2018.03.065

    Article  CAS  PubMed  Google Scholar 

  42. He Q, Song J, Zhang W, Gao S, Wang H, Yu J (2020) Enhanced simultaneous nitrification, denitrification and phosphorus removal through mixed carbon source by aerobic granular sludge. J Hazard Mater 382:121043. https://doi.org/10.1016/j.jhazmat.2019.121043

    Article  CAS  PubMed  Google Scholar 

  43. Rajta A, Bhatia R, Setia H, Pathania P (2020) Role of heterotrophic aerobic denitrifying bacteria in nitrate removal from wastewater. J Appl Microbiol 128:1261–1278. https://doi.org/10.1111/jam.14476

    Article  CAS  PubMed  Google Scholar 

  44. Zhao B, Tian M, An Q, Ye J, Guo JS (2017) Characteristics of a heterotrophic nitrogen removal bacterium and its potential application on treatment of ammonium-rich wastewater. Bioresour Technol 226:46–54. https://doi.org/10.1016/j.biortech.2016.11.120

    Article  CAS  PubMed  Google Scholar 

  45. Qu D, Wang C, Wang Y, Zhou R, Ren H (2015) Heterotrophic nitrification and aerobic denitrification by a novel groundwater origin cold-adapted bacterium at low temperatures. RSC Adv 5:5149–5157. https://doi.org/10.1039/c4ra13141j

    Article  CAS  Google Scholar 

  46. Chen J, Xu J, Zhang S, Liu F, Peng J, Peng Y, Wu J (2021) Nitrogen removal characteristics of a novel heterotrophic nitrification and aerobic denitrification bacteria, Alcaligenes faecalis strain WT14. J Environ Manage 282:111961. https://doi.org/10.1016/j.jenvman.2021.111961

    Article  CAS  PubMed  Google Scholar 

  47. Li L, Zhang J, Tian Y, Zhan W, Lin Q, Li H, Zuo W (2019) Optimization of nutrient removal of novel electrochemically active carriers by response surface methodology. Bioresour Technol 292:122000. https://doi.org/10.1016/j.biortech.2019.122000

    Article  CAS  PubMed  Google Scholar 

  48. Rout PR, Bhunia P, Dash RR (2017) Simultaneous removal of nitrogen and phosphorous from domestic wastewater using Bacillus cereus GS-5 strain exhibiting heterotrophic nitrification, aerobic denitrification and denitrifying phosphorous removal. Bioresour Technol 244:484–495. https://doi.org/10.1016/j.biortech.2017.07.186

    Article  CAS  PubMed  Google Scholar 

  49. Yang J, Feng L, Pi S, Cui D, Ma F, Zhao HP, Li A (2020) A critical review of aerobic denitrification: Insights into the intracellular electron transfer. Sci Total Environ 731:139080. https://doi.org/10.1016/j.scitotenv.2020.139080

    Article  CAS  PubMed  Google Scholar 

  50. Padhi SK, Tripathy S, Sen R, Mahapatra AS, Mohanty S, Maiti NK (2013) Characterisation of heterotrophic nitrifying and aerobic denitrifying Klebsiella pneumoniae CF-S9 strain for bioremediation of wastewater. Int Biodeter Biodegr 78:67–73. https://doi.org/10.1016/j.ibiod.2013.01.001

    Article  CAS  Google Scholar 

  51. Li C, Yang J, Wang X, Wang E, Li B, He R, Yuan H (2015) Removal of nitrogen by heterotrophic nitrification-aerobic denitrification of a phosphate accumulating bacterium Pseudomonas stutzeri YG-24. Bioresour Technol 182:18–25. https://doi.org/10.1016/j.biortech.2015.01.100

    Article  CAS  PubMed  Google Scholar 

  52. Fidelis Silva LC, Santiago Lima H, de Oliveira Mendes TA, Sartoratto A, de Paula SM, de Souza RS, de Paula SO, de Oliveira VM, da Silva CM (2019) Heterotrophic nitrifying/aerobic denitrifying bacteria: ammonium removal under different physical-chemical conditions and molecular characterization. J Environ Manag 248:109294. https://doi.org/10.1016/j.jenvman.2019.109294

    Article  CAS  Google Scholar 

  53. Feng L, Yang J, Yu H, Lan Z, Ye X, Yang G, Yang Q, Zhou J (2020) Response of denitrifying community, denitrification genes and antibiotic resistance genes to oxytetracycline stress in polycaprolactone supported solid-phase denitrification reactor. Bioresour Technol 308:123274. https://doi.org/10.1016/j.biortech.2020.123274

    Article  CAS  PubMed  Google Scholar 

  54. Mauffrey F, Cucaita A, Constant P, Villemur R (2017) Denitrifying metabolism of the methylotrophic marine bacterium Methylophaga nitratireducenticrescens strain JAM1. PeerJ 5:e4098. https://doi.org/10.7717/peerj.4098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Gaimster H, Alston M, Richardson DJ, Gates AJ, Rowley G (2018) Transcriptional and environmental control of bacterial denitrification and N2O emissions. FEMS Microbiol Lett 365:1–19. https://doi.org/10.1093/femsle/fnx277

    Article  CAS  Google Scholar 

  56. Yao S, Ni J, Ma T, Li C (2013) Heterotrophic nitrification and aerobic denitrification at low temperature by a newly isolated bacterium, Acinetobacter sp. HA2. Bioresour Technol 139:80–86. https://doi.org/10.1016/j.biortech.2013.03.189

    Article  CAS  PubMed  Google Scholar 

  57. Man Q, Zhang P, Huang W, Zhu Q, He X, Wei D (2021) A heterotrophic nitrification-aerobic denitrification bacterium Halomonas venusta TJPU05 suitable for nitrogen removal from high-salinity wastewater. Front Env Sci Eng 16:1–10. https://doi.org/10.1007/s11783-021-1503-6

    Article  CAS  Google Scholar 

  58. Qiao Z, Wu Y, Qian J, Hu S, Chan J, Liu X, Sun R, Wang W, Zhou B (2020) A lab-scale study on heterotrophic nitrification-aerobic denitrification for nitrogen control in aquatic ecosystem. Environ Sci Pollut Res 27:9307–9317. https://doi.org/10.1007/s11356-019-07551-3

    Article  CAS  Google Scholar 

  59. Xing CY, Fan YC, Chen X, Guo JS, Shen Y, Yan P, Fang F, Chen YP (2020) A self-assembled nanocompartment in anammox bacteria for resisting intracelluar hydroxylamine stress. Sci Total Environ 717:137030. https://doi.org/10.1016/j.scitotenv.2020.137030

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was financially supported by the Shenyang Science and Technology Plan Fund Project (No. 21-108-9-25), China Major Science and Technology Program for Water Pollution Control and Treatment (No. 2018ZX07601-002), and the Liaoning Doctoral Research Start-up Fund (No.2019-BS-087).

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Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Eco-restoration of Regional Contaminated Environment, Shenyang University, Shenyang, 110044, Liaoning, China

    Yihua Dong, Ziyang Wang, Xueying Zhang & Feng Chen

  2. School of Resources and Civil Engineering, Northeastern University, Shenyang, 110819, Liaoning, China

    Liang Li

  3. China Urban Construction Design Environmental Technology Co. Ltd, Beijing, 100120, China

    Jianghai He

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DY-H: conceptualization, funding acquisition, investigation, visualization, methodology, writing—review and editing. WZ-Y: investigation, writing—original draft. LL: conceptualization, supervision, review and editing, funding acquisition. ZX–Y: investigation, writing—original draft. CF: investigation, writing—review and editing. HJ-H: writing—review and editing. All authors read and approved the final manuscript.

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Dong, Y., Wang, Z., Li, L. et al. Heterotrophic nitrification and aerobic denitrification characteristics of the psychrotolerant Pseudomonas peli NR-5 at low temperatures. Bioprocess Biosyst Eng 46, 693–706 (2023). https://doi.org/10.1007/s00449-023-02854-9

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