Growth optimization of Klebsiella pneumoniae in magnetically assisted bioreactor

• Autorzy: Konopacki Maciej , Augustyniak Adrian , Grygorcewicz Bartłomiej , Dołęgowska Barbara , Kordas Marian , Rakoczy Rafał

Identyfikatory

DOI

10.24425/cpe.2022.140833

• Języki publikacji: EN

Abstrakty

EN

In recent years, infections are more often caused by pathogens with high multi-drug resistance, classified as the “ESKAPE” microorganisms. Therefore, investigation of these pathogens, e.g., Klebsiella pneumoniae, often requires biomass production for treatment testing such as antibiotics or bacteriophages. Moreover, K. pneumoniae can be successfully applied as a biocatalyst for other industrial applications, increasing the need for this bacteria biomass. In the current study, we proposed a novel magnetically assisted bioreactor for the cultivation of K. pneumoniae cells in the presence of an external alternating magnetic field (AMF). High efficiency of the production requires optimal bacteria growth conditions, e.g., temperature and field frequency. Therefore, we performed an optimization procedure using a central composite design for these two parameters in a wide range. As an objective function, we utilized a novel, previously described growth factor that considers both biomass and bacteria growth kinetics. Thus, based on the response surface, we could specify the optimal growth conditions. Moreover, we analysed the impact of the AMF on bacteria proliferation, which indicated positive field frequency windows, where the highest stimulatory effect of AMF on bacteria proliferation occurred. Obtained results proved that the magnetically assisted bioreactor could be successfully employed for K. pneumoniae cultivation.

Słowa kluczowe

EN

bacteria cultivation; growth kinetics; optimization process; magnetically assisted bioreactor

PL

hodowla bakterii; kinetyka wzrostu; proces optymalizacji; bioreaktor wspomagany magnetycznie

• Wydawca: Komitet Inżynierii Chemicznej i Procesowej Polskiej Akademii Nauk
• Czasopismo: Chemical and Process Engineering
• Rocznik: 2022
• Tom: Vol. 43, nr 3
• Strony: 289–--304
• Opis fizyczny: Bibliogr. 44 poz., wykr., rys.

Twórcy

autor

Konopacki Maciej

• West Pomeranian University of Technology in Szczecin, Faculty of Chemical Technology and Engineering, Department of Chemical and Process Engineering, al. Piastów 42, 71-065 Szczecin, Poland
• Pomeranian Medical University in Szczecin, Chair of Microbiology, Immunology and Laboratory Medicine, Department of Laboratory Medicine, al. Powstańców Wielkopolskich 72, 70-111 Szczecin, Poland

• https://orcid.org/0000-0002-2240-7317

autor

Augustyniak Adrian

• West Pomeranian University of Technology in Szczecin, Faculty of Chemical Technology and Engineering, Department of Chemical and Process Engineering, al. Piastów 42, 71-065 Szczecin, Poland
• Technische Universität Berlin, Building Materials and Construction Chemistry, Gustav-Meyer Allee 25, 13355 Berlin, Germany

• https://orcid.org/0000-0001-6636-9909

autor

Grygorcewicz Bartłomiej

• West Pomeranian University of Technology in Szczecin, Faculty of Chemical Technology and Engineering, Department of Chemical and Process Engineering, al. Piastów 42, 71-065 Szczecin, Poland
• Pomeranian Medical University in Szczecin, Chair of Microbiology, Immunology and Laboratory Medicine, Department of Laboratory Medicine, al. Powstańców Wielkopolskich 72, 70-111 Szczecin, Poland

• https://orcid.org/0000-0002-0593-0069

autor

Dołęgowska Barbara

• Pomeranian Medical University in Szczecin, Chair of Microbiology, Immunology and Laboratory Medicine, Department of Laboratory Medicine, al. Powstańców Wielkopolskich 72, 70-111 Szczecin, Poland

• https://orcid.org/0000-0003-3138-1013

autor

Kordas Marian

• West Pomeranian University of Technology in Szczecin, Faculty of Chemical Technology and Engineering, Department of Chemical and Process Engineering, al. Piastów 42, 71-065 Szczecin, Poland

• https://orcid.org/0000-0001-9982-1658

autor

Rakoczy Rafał

• West Pomeranian University of Technology in Szczecin, Faculty of Chemical Technology and Engineering, Department of Chemical and Process Engineering, al. Piastów 42, 71-065 Szczecin, Poland

• https://orcid.org/0000-0002-5770-926X

Bibliografia

• 1. Ahmed I., Istivan T., Cosic I., Pirogova E., 2013. Evaluation of the effects of Extremely Low Frequency (ELF) Pulsed Electromagnetic Fields (PEMF) on survival of the bacterium Staphylococcus aureus. EPJ Nonlinear Biomed. Phys., 1, 5. DOI: 10.1140/epjnbp12.
• 2. Al-Qodah Z., Al-Shannag M., Al-Busoul M., Penchev I., Orfali W., 2017. Immobilized enzymes bioreactors utilizing a magnetic field: A review. Biochem. Eng. J., 121, 94–106. DOI: 10.1016/j.bej.2017.02.003.
• 3. Askitosari T.D., Boto S.T., Blank L.M., Rosenbaum M.A., 2019. Boosting heterologous phenazine production in Pseudomonas putida KT2440 through the exploration of the natural sequence space. Front. Microbiol., 10, 1990. DOI: 10.3389/fmicb.2019.01990.
• 4. Aubert G., Jacquinot J.-F., Sakellariou D., 2012. Eddy current effects in plain and hollow cylinders spinning inside homogeneous magnetic fields: Application to magnetic resonance. J. Chem. Phys., 137, 154201. DOI: 10.1063/1.4756948.
• 5. Augustyniak A., Sikora P., Jabłońska J., Cendrowski K., John E., Stephan D., Mijowska E., 2020. The effects of calcium–silicate–hydrate (C–S–H) seeds on reference microorganisms. Appl. Nanosci., 10, 4855–4867. DOI: 10.1007/s13204-020-01347-5.
• 6. Binhi V.N., Savin A.V., 2002. Molecular gyroscopes and biological effects of weak extremely low-frequency magnetic fields. Phys. Rev. E, 65, 051912. DOI: 10.1103/PhysRevE.65.051912.
• 7. Carta R., Desogus F., 2012. Possible non-thermal microwave effects on the growth rate of Pseudomonas Aeruginosa and Staphylococcus Aureus. Int. Rev. Chem. Eng., 4(4), 392–398.
• 8. Chen Z., Sun H., Huang J., Wu Y., Liu D., 2015. Metabolic engineering of Klebsiella pneumoniae for the production of 2-butanone from glucose. PLoS ONE, 10, e0140508. DOI: 10.1371/journal.pone.0140508.
• 9. de Andrade C.M., Cogo A.J.D., Perez V.H., dos Santos N.F., Okorokova-Façanha A.L., Justo O.R., Façanha A.R., 2021. Increases of bioethanol productivity by S. cerevisiae in unconventional bioreactor under ELF-magnetic field: New advances in the biophysical mechanism elucidation on yeasts. Renewable Energy, 169, 836–842. DOI: 10.1016/j.renene.2021.01.074.
• 10. Derakhshandeh M., Tezcan Un U., 2019. Optimization of microalgae Scenedesmus SP. growth rate using a central composite design statistical approach. Biomass Bioenergy, 122, 211–220. DOI: 10.1016/j.biombioe.2019.01.022.
• 11. Domingues L., Vicente A.A., Lima N., Teixeira J.A., 2000. Applications of yeast flocculation in biotechnological processes. Biotechnol. Bioprocess Eng., 5, 288–305. DOI: 10.1007/BF02942185.
• 12. Fijałkowski K., Żywicka A., Drozd R., Junka A.F., Peitler D., Kordas M., Konopacki M., Szymczyk P., El Fray M., Rakoczy R., 2016. Increased yield and selected properties of bacterial cellulose exposed to different modes of a rotating magnetic field. Eng. Life Sci., 16, 483–493. DOI: 10.1002/elsc.201500151.
• 13. Grimont P.A.D., Grimont F., 2015. Klebsiella, In: Whitman W.B. et al. (Eds.), Bergey’s manual of systematics of archaea and bacteria. Willey, New York, 1–26. DOI: 10.1002/9781118960608.gbm01150.
• 14. Grygorcewicz B., Chajęcka-Wierzchowska W., Augustyniak A., Wasak A., Stachurska X., Nawrotek P., Dołęgowska B., 2020. In-milk inactivation of Escherichia coli O157:H7 by the environmental lytic bacteriophage ECPS-6. J. Food Saf., 40, e12747. DOI: 10.1111/jfs.12747.
• 15. Grygorcewicz B., Grudziński M., Wasak A., Augustyniak A., Pietruszka A., Nawrotek P., 2017. Bacteriophage-mediated reduction of Salmonella Enteritidis in swine slurry. Appl. Soil Ecol., 119, 179–182. DOI: 10.1016/j.apsoil.2017.06.020.
• 16. Hall M.D., Simeonov A., Davis M.I., 2016. Avoiding fluorescence assay interference-The case for diaphorase. ASSAY Drug Dev. Technol., 14, 3, 175–179. DOI: 10.1089/adt.2016.707.
• 17. Hammond P., 1962. The calculation of the magnetic field of rotating machines. Part 3: Eddy currents induced in a solid slab by a circular current loop. Proc. IEE – Part C: Monographs, 109, 508–515. DOI: 10.1049/pic.1962.0066.
• 18. Hristov J., 2010. Magnetic field assisted fluidization – a unified approach.Part 8. Mass transfer: Magnetically assisted bioprocesses. Rev. Chem. Eng., 26, 55–128. DOI: 10.1515/REVCE.2010.006.
• 19. Jabłońska J., Augustyniak A., Kordas M., Dubrowska K., Sołoducha D., Borowski T., Konopacki M., Grygorcewicz B., Roszak M., Dołęgowska B., Piz M., Filipek E., Wróbel R.J., Leniec G., Rakoczy R., 2022. Evaluation of ferrofluid-coated rotating magnetic field-assisted bioreactor for biomass production. Chem. Eng. J., 431, 133913. DOI: 10.1016/J.CEJ.2021.133913.
• 20. Kollef M.H., Chastre J., Fagon J.-Y., François B., Niederman M.S., Rello J., Torres A., Vincent J.-L., Wunderink R.G., Go K.W., Rehm C., 2014. Global prospective epidemiologic and surveillance study of ventilator-associated pneumonia due to Pseudomonas aeruginosa*. Crit. Care Med., 42, 2178–2187. DOI: 10.1097/CCM.0000000000000510.
• 21. Konopacka A., Rakoczy R., Konopacki M., 2019. The effect of rotating magnetic field on bioethanol production by yeast strain modified by ferrimagnetic nanoparticles. J. Magn. Magn. Mater., 473, 176–183. DOI: 10.1016/j.jmmm.2018.10.053.
• 22. Konopacki M., Augustyniak A., Grygorcewicz B., Dołęgowska, B., Kordas, M., Rakoczy R. 2020. Single mathematical parameter for evaluation of the microorganisms’ growth as the objective function in the optimization by the doe techniques. Microorganisms, 8, 1706. DOI: 10.3390/microorganisms8111706.
• 23. Konopacki M., Rakoczy R., 2019. The analysis of rotating magnetic field as a trigger of Gram-positive and Gram-negative bacteria growth. Biochem. Eng. J., 141, 259–267. DOI: 10.1016/j.bej.2018.10.026
• 24. Konopacki, M., Jędrzejczak-Silicka, M., Szymańska, K., Mijowska, E., Rakoczy, R., 2021. Effect of rotating magnetic field on ferromagnetic structures used in hyperthermia. J. Magn. Magn. Mater., 518, 167418. DOI: 10.1016/j.jmmm.2020.167418.
• 25. Kumar V., Park S., 2018. Potential and limitations of Klebsiella pneumoniae as a microbial cell factory utilizing glycerol as the carbon source. Biotechnol. Adv., 36, 150–167. DOI: 10.1016/j.biotechadv.2017.10.004.
• 26. Lechowska J., Kordas M., Konopacki M., Fijałkowski K., Drozd R., Rakoczy R., 2019. Hydrodynamic studies in magnetically assisted external-loop airlift reactor. Chem. Eng. J., 362, 298–309. DOI: 10.1016/j.cej.2019.01.037.
• 27. Leili M., Shirmohammadi K.N., Godini K., Azarian G., Moussavi R., Peykhoshian A., 2020. Application of central composite design (CCD) for optimization of cephalexin antibiotic removal using electro-oxidation process. J. Mol. Liq., 313, 113556. DOI: 10.1016/j.molliq.2020.113556.
• 28. Lemire J., Alhasawi A., Appanna V.P., Tharmalingam S., Appanna V.D., 2017. Metabolic defence against oxidative stress: the road less travelled so far. J. Appl. Microbiol., 123, 798–809. DOI: 10.1111/jam.13509.
• 29. Medina-Cabrera E.V., Rühmann B., Schmid J., Sieber V., 2020. Optimization of growth and EPS production in two Porphyridum strains. Bioresour. Technol. Rep., 11, 100486. DOI: 10.1016/j.biteb.2020.100486.
• 30. Mitrea L., Vodnar, D.C., 2019. Klebsiella pneumoniae – a useful pathogenic strain for biotechnological purposes: Diols biosynthesis under controlled and uncontrolled pH levels. Pathogens, 8, 293. DOI: 10.3390/pathogens8040293.
• 31. Qin J., Xiao Z., Ma C., Xie N., Liu P., Xu P., 2006. Production of 2,3-butanediol by Klebsiella Pneumoniae using glucose and ammonium phosphate. Chin. J. Chem. Eng., 14, 132–136. DOI: 10.1016/S1004-9541(06)60050-5.
• 32. Rakoczy R., Lechowska J., Kordas M., Konopacki M., Fijałkowski K., Drozd R., 2017a. Effects of a rotating magnetic field on gas-liquid mass transfer coefficient. Chem. Eng. J., 327, 608–617. DOI: 10.1016/j.cej.2017.06.132.
• 33. Rakoczy R., Przybył A., Kordas M., Konopacki M., Drozd R., Fijałkowski K., 2017b. The study of influence of a rotating magnetic field on mixing efficiency. Chem. Eng. Process. Process Intensif., 112, 1–8. DOI: 10.1016/j.cep.2016.12.001.
• 34. Rehman S., Khairul I.M., Khalid K.N., Kyoungjin A.A., Chaiprapat S., Leu, S.Y., 2021. Whole sugar 2,3-butanediol fermentation for oil palm empty fruit bunches biorefinery by a newly isolated Klebsiella pneumoniae PM2. Bioresour. Technol., 333, 125206. DOI: 10.1016/j.biortech.2021.125206.
• 35. Roger M., Brown F., Gabrielli W., Sargent F., 2018. Efficient hydrogen-dependent carbon dioxide reduction by Escherichia coli. Curr. Biol., 28, 140–145. DOI: 10.1016/j.cub.2017.11.050.
• 36. Sabra W., Groeger C., Zeng A.P., 2016. Microbial cell factories for diol production, In: Ye Q., Bao J., Zhong J.J. (Eds.), Bioreactor engineering research and industrial applications I. Advances in biochemical engineering/biotechnology. Springer, Berlin, Heidelberg. 155, 165–197. DOI: 10.1007/10_2015_330.
• 37. Santini S.J., Cordone V., Falone S., Mijit M., Tatone C., Amicarelli F., Di Emidio G., 2018. Role of mitochondria in the oxidative stress induced by electromagnetic fields: Focus on reproductive systems. Oxid. Med. Cell. Longevity, 2018, 5076271. DOI: 10.1155/2018/5076271.
• 38. Struk M., Grygorcewicz B., Nawrotek P., Augustyniak A., Konopacki M., Kordas M., Rakoczy R., 2017. Enhancing effect of 50 Hz rotating magnetic field on induction of Shiga toxin-converting lambdoid prophages. Microb. Pathogen., 109, 4–7. DOI: 10.1016/j.micpath.2017.05.018.
• 39. Sun S., Shu L., Lu X., Wang Q., Tišma M., Zhu C., Shi J., Baganz F., Lye G.J., Hao, J., 2021. 1,2–Propanediol production from glycerol via an endogenous pathway of Klebsiella pneumoniae. Appl. Microbiol. Biotechnol.,105, 23, 9003–9016. DOI: 10.1007/s00253-021-11652-w.
• 40. Sybesma W., Zbinden R., Chanishvili N., Kutateladze M., Chkhotua A., Ujmajuridze A., Mehnert U., Kessler T.M., 2016. Bacteriophages as potential treatment for urinary tract infections. Front. Microbiol., 7, 465, 1–9. DOI: 10.3389/fmicb.2016.00465.
• 41. Tacconelli E., Carrara E., Savoldi A., Harbarth S., Mendelson M., Monnet D.L., Pulcini C., Kahlmeter G., Kluytmans J., Carmeli Y., Ouellette M., Outterson K., Patel J., Cavaleri M., Cox E.M, Houchens C.R, Grayson M.L., Hansen P., Singh N., Theuretzbacher U., Magrini N., The WHO Pathogens Priority List Working Group, 2018. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect. Dis., 18, 318-327. DOI: 10.1016/S1473-3099(17)30753-3
• 42. Wang Z., Liu X., Ni S.Q., Zhang J., Zhang X., Ahmad H.A., Gao B., 2017. Weak magnetic field: A powerful strategy to enhance partial nitrification. Water Res., 120, 190–198. DOI: 10.1016/j.watres.2017.04.058.
• 43. Zhang X., Yarema K., Xu A., 2017. Impact of static magnetic field (SMF) on microorganisms, plants and animals. In: Biological effects of static magnetic fields. Springer Singapore, 133–172. DOI: 10.1007/978-981-10-3579-1.
• 44. Zwietering M.H., Jongenburger I., Rombouts F.M., van’t Riet K., 1990. Modeling of the bacterial growth curve. Appl. Environ. Microbiol., 56, 1875–1881. DOI: 10.1128/aem.56.6.1875-1881.1990.