Medical Radiology and Radiation Safety. 2025. Vol. 70. № 1
DOI:10.33266/1024-6177-2025-70-1-21-29
A.V. Gutnov1, O.V. Belov2, G.S. Kachmazov1, T.T. Magkoev1,
N.R. Popova3, N.E. Pukhaeva 1, 2
The Effect of Heavy Ion Irradiation on the Metabolism of Technologically and Biologically Significant Microorganisms: Biotechnological Prospects of Application
1 North Ossetian State University, Vladikavkaz, Russia
2 Joint Institute for Nuclear Research, Dubna, Russia
3 Institute of Theoretical and Experimental Biophysics, Pushchino, Russia
Contact person: A.V. Gutnov, e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.
ABSTRACT
Purpose: To review the literature on the use of heavy ion beam mutagenesis for selecting various microorganisms, including bacteria, fungi, yeast, and microalgae, for biotechnological purposes.
Material and methods: Data have been collected over the past 15 years on the metabolic effects of mutants exposed to heavy ions, biotechnologically significant microbiological objects (bacteria, fungi, algae).
Results and discussion: The biotechnological and genetic significance, as well as the morphological and other aspects of the detected changes in mutant microbiological objects, are discussed. Currently, heavy ion irradiation-induced mutagenesis with high linear energy transfer and biological efficiency is recognized as a powerful new method for creating microbial strains with previously unknown properties. We believe that targeted breeding using heavy ion mutagenesis will make a significant contribution to the development of industrial producer strains for biotechnology.
Conclusion: The studies discussed in this review indicate that the use of ion beam mutagenesis for microorganisms can be beneficial for both fundamental science and applied research.
Keywords: biotechnology, microorganisms, metabolism, mutagenesis, heavy ion irradiation
For citation: Gutnov AV, Belov OV, Kachmazov GS, Magkoev TT, Popova NR, Pukhaeva NE. The Effect of Heavy Ion Irradiation on the Metabolism of Technologically and Biologically Significant Microorganisms: Biotechnological Prospects of Application. Medical Radiology and Radiation Safety. 2025;70(1):21–29. (In Russian). DOI:10.33266/1024-6177-2025-70-1-21-29
References
1. Saa P.A. Rational Metabolic Pathway Prediction and Design: Computational Tools and Their Applications for Yeast Systems and Synthetic Biology. Synthetic Biology of Yeasts. Ed. Darvishi Harzevili F. Springer, Cham, 2022. P. 2-25. doi.org/10.1007/978-3-030-89680-5_1.
2. Huttanus H.M., Triola E-K.H., Velasquez-Guzman J.C., Shin S.-M., Granja-Travez RS, Singh A., Dale T., Jha R.K. Targeted Mutagenesis and High-Throughput Screening of Diversified Gene and Promoter Libraries for Isolating Gain-of-Function Mutations. Front. Bioeng. Biotechnol. 2023;11:1202388. doi: 10.3389/fbioe.2023.1202388.
3. Guo X., Ren J., Zhou X., Zhang M., Lei C., Chai R., Lu D. Strategies to Improve the Efficiency and Quality of Mutant Breeding Using Heavy-Ion Beam Irradiation. Critical Reviews in Biotechnology. 2023;44;5:735–752. doi.org/10.1080/07388551.2023.2226339.
4. Hirano T., Kazama Y., Ishii K., Ohbu S., Shirakawa Y., Abe T. Comprehensive Identification of Mutations Induced by Heavy-Ion Beam Irradiation in Arabidopsis Thaliana. The Plant Journal. 2015; 82;1:93-104. doi.org/10.1111/tpj.12793.
5. Aroumougame A., David J. Chen. Mechanism of Cluster DNA Damage Repair in Response to High-Atomic Number and Energy Particles Radiation. Mutation Research. Fundamental and Molecular Mechanisms of Mutagenesis. 2011;711;1–2:87-99. doi.org/10.1016/j.mrfmmm.2010.11.002.
6. Du Y., Zou W., Zhang K., Ye G., Yang J. Advances and Applications of Clostridium Co-culture Systems in Biotechnology. Front. Microbiol. 2020;11:560223. doi:10.3389/fmicb.2020.560223.
7. Yuchen Liu, Yan Yuan, Ganesan Ramya, Shiv Mohan Singh, Nguyen Thuy Lan Chi, Arivalagan Pugazhendhi, Changlei Xia, Thangavel Mathimani. A Review on the Promising Fuel of the Future – Biobutanol; the Hindrances and Future Perspectives. Fuel. 2022;327:125166. doi.org/10.1016/j.fuel.2022.125166.
8. Cansu Birgen, Peter Dürre, Heinz A. Preisig, Alexander Wentzel. Butanol Production from Lignocellulosic Biomass: Revisiting Fermentation Performance Indicators with Exploratory Data Analysis. Biotechnol Biofuels. 2019;12:167. doi.org/10.1186/s13068-019-1508-6.
9. Zhou X., Lu X.H., Li X.H., et al. Radiation Induces Acid Tolerance of Clostridium Tyrobutyricum and Enhances Bioproduction of Butyric Acid through a Metabolic Switch. Biotechnol Biofuels. 2014;7:22. doi.org/10.1186/1754-6834-7-22.
10. Gao Y., Zhang M., Zhou X., Guo X., Lei C., Li W., Lu D. Effects of Carbon Ion Beam Irradiation on Butanol Tolerance and Production of Clostridium Acetobutylicum. Front. Microbiol. 2020;11:602774. doi: 10.3389/fmicb.2020.602774.
11. Li H.G., Luo W., Gu Q.Y., Wang Q., Hu W.-J., Yu X.B. Acetone, Butanol and Ethanol Production from Cane Molasses Using Clostridium Beijerinckii Mutant Obtained by Combined Low-Energy Ion Beam Implantation and N-Methyl-N-Nitro-N-Nitrosoguanidine Induction. Bioresource. Technol. 2013;137:254–260. doi: 10.1016/j.biortech.2013.03.084.
12. Jinshui Zheng, Stijn Wittouck, Elisa Salvetti, Charles M.A.P. Franz, Hugh M.B. Harris, Paola Mattarelli, Paul W. O’Toole, Bruno Pot, Peter Vandamme, Jens Walter, Koichi Watanabe, Sander Wuyts, Giovanna E. Felis, Michael G. Gänzl, Sarah Lebeer. A Taxonomic Note on the Genus Lactobacillus: Description of 23 Novel Genera, Emended Description of the Genus Lactobacillus Beijerinck 1901, and Union of Lactobacillaceae and Leuconostocaceae. International Journal of Systematic and Evolutionary Microbiology. 2020;70;4:2782–2858. doi.org/10.1099/ijsem.0.004107.
13. Ashfaq Ahmad, Fawzi Banat, Hanifa Taher. A Review on the Lactic acid Fermentation from Low-Cost Renewable Materials: Recent Developments and Challenges. Environmental Technology & Innovation. 2020;20:101138. doi.org/10.1016/j.eti.2020.101138.
14. Jiang A.L., Hu W., Li W.-J., Liu L., Tian X.-J., Liu J., Wang S.-Y., Lu D., Chen J.-H. Enhanced Production of L-Lactic Acid by Lactobacillus Thermophilus SRZ50 Mutant Generated by High-Linear Energy Transfer Heavy Ion Mutagenesis. Eng. Life Sci. 2018;18:626-634. doi.org/10.1002/elsc.201800052.
15. Cerna-Chávez E., Rodríguez-Rodríguez J.F., García-Conde K.B., Ochoa-Fuentes Y.M. Potential of Streptomyces Avermitilis: a Review on Avermectin Production and Its Biocidal Effect. Metabolites. 2024;14:374. doi.org/10.3390/metabo14070374.
16. Seung Bum Kim, Michael Goodfellow. Streptomyces Avermitilis Sp. Nov., Nom. Rev., a Taxonomic Home for the Avermectin-Producing Streptomycetes. International Journal of Systematic and Evolutionary Microbiology. 2002;52:2011–2014. https://doi.org/10.1099/00207713-52-6-2011.
17. El-Saber Batiha G., Alqahtani A., Ilesanmi O.B., Saati A.A., El-Mleeh A., Hetta H.F., Magdy Beshbishy A. Avermectin Derivatives, Pharmacokinetics, Therapeutic and Toxic Dosages, Mechanism of Action, and Their Biological Effects. Pharmaceuticals. 2020;13:196. doi.org/10.3390/ph13080196.
18. Wang, Shu-Yang, Bo, Yong-Heng, Zhou, Xiang, Chen, Ji-Hong, Li, Wen-Jian, Liang, Jian-Ping, Xiao, Guo-Qing, Wang, Yu-Chen, Liu, Jing, Hu, Wei, Jiang, Bo-Ling. Significance of Heavy-Ion Beam Irradiation-Induced Avermectin B1a Production by Engineered Streptomyces Avermitilis. BioMed Research International. 2017;5373262:13. doi.org/10.1155/2017/5373262.
19. Alam K., Mazumder A., Sikdar S., Zhao Y.M., Hao J., Song C., Wang Y., Sarkar R., Islam S., Zhang Y., Li A. Streptomyces: the Biofactory of Secondary Metabolites. Front. Microbiol. 2022;13:968053. https://doi.org/10.3389%2Ffmicb.2022.968053.
20. Fang Xiao, Tiyanont Kittichoat, Zhang Yi, Wanner Jutta, Boger Dale, Walker Suzanne. The Mechanism of Action of Ramoplanin and Enduracidin. Mol. BioSyst. 2006;2;1:69-76. doi.org/10.1039/B515328J.
21. Lu Liu, Wei Hu, Wen-jian Li, Shu-yang Wang, Dong Lu, Xue-jiao Tian, Yan-qin Mao, Jing Liu, Ji-hong Chen. Heavy-Ion Mutagenesis Significantly Enhances Enduracidin Production by Streptomyces Fungicidicus. Eng. Life Sci. 2019;19:112–120. doi.org/10.1002/elsc.201800109.
22. Gharibzahedi S.M.T., Razavi S.H., Mousavi S.M. Characterization of Bacteria of the Genus Dietzia: an Updated Review. Ann. Microbiol. 2014;64:1–11. doi.org/10.1007/s13213-013-0603-3.
23. Esatbeyoglu T., Rimbach G. Canthaxanthin: from Molecule to Function. Mol. Nutr. Food Res. 2017;61;6. doi.org/10.1002/mnfr.201600469.
24. Faramarz Khodaiyan, Seyed Hadi Razavi, Seyed Mohammad Mousavi. Optimization of Canthaxanthin Production by Dietzia Natronolimnaea HS-1 from Cheese whey Using Statistical Experimental Methods. Biochemical Engineering Journal. 2008;40;3:415-422. doi.org/10.1016/j.bej.2008.01.016.
25. Zhou X., Xie J.R., Tao L., et al. The Effect of Microdosimetric 12C6+ Heavy Ion Irradiation and Mg2+ on Canthaxanthin Production in a Novel Strain of Dietzia Natronolimnaea. BMC Microbiol. 2013;13:213. doi.org/10.1186/1471-2180-13-213.
26. Tobert J. Lovastatin and Beyond: the History of the HMG-CoA Reductase Inhibitors. Nat. Rev. Drug. Discov. 2003;2:517–526. doi.org/10.1038/nrd1112.
27. Lass-Flörl C., Dietl A., Kontoyiannis D.P., Brock M. Aspergillus Terreus Species Complex. Clin. Microbiol. Rev. 2021;34:e00311-20. doi.org/10.1128/CMR.00311-20
28. Goswami S., Vidyarthi A.S., Bhunia B., Mandal T. A Review on Lovastatin and its Production. J. Biochem. Tech. 2012;4;1:581-587.
29. Li S.W., Li M., Song H.P., et al. Induction of a High-Yield Lovastatin Mutant of Aspergillus Terreus by 12C6+ Heavy-Ion Beam Irradiation and the Influence of Culture Conditions on Lovastatin Production Under Submerged Fermentation. Appl. Biochem. Biotechnol. 2011;165:913–925. doi.org/10.1007/s12010-011-9308-x.
30. Behera B.C. Citric Acid from Aspergillus Niger: a Comprehensive Overview. Critical Reviews in Microbiology. 2020;46;6:727–749. doi.org/10.1080/1040841X.2020.1828815.
31. Marin Berovic, Matic Legisa. Citric Acid Production. Biotechnology Annual Review. 2007;13:303-343. doi.org/10.1016/S1387-2656(07)13011-8.
32. Hu W., Liu J., Chen Jh., et al. A Mutation of Aspergillus Niger for Hyper-Production of Citric Acid from Corn Meal Hydrolysate in a Bioreactor. J. Zhejiang Univ. Sci. B. 2014;15:1006–1010. doi.org/10.1631/jzus.B1400132.
33. Jiang B.L., Wang S.Y., Wang Y.C., et al. A High-Throughput Screening Method for Breeding Aspergillus Niger with 12C6+ Ion Beam-Improved Cellulase. Nucl Sci Tech. 2017;28:1. doi.org/10.1007/s41365-016-0157-8.
34. Xiaoyu Ma, Ming Gao, Yuan Li, Qunhui Wang, Xiaohong Sun. Production of Cellulase by Aspergillus Niger through Fermentation of Spent Mushroom Substance: Glucose Inhibition and Elimination Approaches. Process Biochemistry. 2022;122;2:26-35. doi.org/10.1016/j.procbio.2022.09.029.
35. Rahul Ranjan, Rohit Rai, Smruti B. Bhatt, Prodyut Dhar. Technological Road Map of Cellulase: a Comprehensive Outlook to Structural, Computational, and Industrial Applications. Biochemical Engineering Journal. 2023;198:109020. doi.org/10.1016/j.bej.2023.109020.
36. Yao X., Guo H., Zhang K., Zhao M., Ruan J., Chen J. Trichoderma and its Role in Biological Control of Plant Fungal and Nematode Disease. Front. Microbiol. 2023;14:1160551. doi.org/10.3389%2Ffmicb.2023.1160551.
37. Zheng Zhang, Jing Xing, Xuezhi Li, Xianqin Lu, Guodong Liu, Yinbo Qu, Jian Zhao. Review of Research Progress on the Production of Cellulase from Filamentous Fungi. International Journal of Biological Macromolecules. 2024;277;4:134539. doi.org/10.1016/j.ijbiomac.2024.134539.
38. Li Z., Chen X., Li Z., et al. Strain Improvement of Trichoderma Viride for Increased Cellulase Production by Irradiation of Electron and 12C6+-Ion Beams. Biotechnol Lett. 2016;38:983–989. doi.org/10.1007/s10529-016-2066-7.
39. Patel A., Karageorgou D., Rova E., Katapodis P., Rova U., Christakopoulos P., Matsakas L. An Overview of Potential Oleaginous Microorganisms and their Role in Biodiesel and Omega-3 Fatty Acid-Based Industries. Microorganisms. 2020;8:434. doi.org/10.3390/microorganisms8030434
40. Kot A.M., Błażejak S., Kurcz A., Gientka I., Kieliszek M. Rhodotorula Glutinis – Potential Source of Lipids, Carotenoids, and Enzymes for Use in Industries. Appl. Microbiol. Biotechnol. 2016;100:6103–6117. https://doi.org/10.1007/s00253-016-7611-8.
41. Wang J., Li R., Lu D., et al. A Quick Isolation Method for Mutants with High Lipid Yield in Oleaginous Yeast. World J. Microbiol. Biotechnol. 2009;25:921–925. doi.org/10.1007/s11274-009-9960-2.
42. Yan Ya-ping, Wang Ju-fang, Lu Dong, Dong Xi-cun, Gao Feng, Ma Liang, Li Wen-jian. Study on Yeast Mutant with High Alcohol Yield Fermented in Sweet Sorghum Juice Using Carbon Ion Irradiation. Nuclear Physics Review. 2009;26;3:269-273. doi:10.11804/NuclPhysRev.26.03.269.
43. José M. Lou-Bonafonte, Roberto Martínez-Beamonte, Teresa Sanclemente, Joaquín C. Surra, Luis V. Herrera-Marcos, Javier Sanchez-Marco, Carmen Arnal, Jesús Osada. Current Insights into the Biological Action of Squalene. Mol. Nutr. Food Res. 2018;62;15:e1800136. doi.org/10.1002/mnfr.201800136.
44. Spanova M., Daum G. Squalene – Biochemistry, Molecular Biology, Process Biotechnology, and Applications. Eur. J. Lipid Sci. Technol. 2011;113:1299-1320. doi.org/10.1002/ejlt.201100203.
45. João Paulo Telles, Victoria Stadler Tasca Ribeiro, Letícia Kraft, Felipe Francisco Tuon. Pseudozyma spp. Human Infections: a Systematic Review. Medical Mycology. 2021;59;1:1–6. doi.org/10.1093/mmy/myaa025.
46. Xiao Yan, Wang Lu, Wang Sen, Cong Peihu, Lu Dong, Feng Yingang, Cui Qiu, Song Xiaojin. Mutation and Selection of High Squalene Production Yeast Pseudozyma sp. Induced by Carbon-Ions Beam Irradiation and its Electrotransformation. South China Fisheries Science. 2022;18;2:98-104. doi:10.12131/20210294.
47. Baisho K., Tomioka H., Furuki Y., Hayashi Y., Abe T. Mutation Breeding of Sake Yeast Using Heavy-Ion-Beam Irradiation. Riken Accel. Prog. Rep. 2019;53:202.
48. Pieter De Brabander, Evelien Uitterhaegen, Tom Delmulle, Karel De Winter, Wim Soetaert. Challenges and Progress Towards Industrial Recombinant Protein Production in Yeasts: a Review. Biotechnology Advances. 2023;64:108121. doi.org/10.1016/j.biotechadv.2023.108121.
49. Liang Ma, Zeya Du, Xiang Zhou, Jihong Chen. Screening and Breeding of High Yield Strain of Protein Feed Yeast and Optimization of its Fermentation Process. Nuclear Physics Review. 2022;39;4:512-518. doi: 10.11804/NuclPhysRev.39.2022063.
50. Ye Y., Liu M., Yu L., Sun H., Liu J. Nannochloropsis as an Emerging Algal Chassis for Light-Driven Synthesis of Lipids and High-Value Products. Mar. Drugs. 2024;22:54. doi.org/10.3390/md22020054.
51. Zhang S., Zhang L., Xu G., Li F., Li X. A Review on Biodiesel Production from Microalgae: Influencing Parameters and Recent Advanced Technologies. Front. Microbiol. 2022;13:970028. doi.org/10.3389%2Ffmicb.2022.970028.
52. Yubin Ma, Zhiyao Wang, Ming Zhu, Changjiang Yu, Yingping Cao, Dongyuan Zhang, Gongke Zhou. Increased Lipid Productivity and TAG Content in Nannochloropsis by Heavy-Ion Irradiation Mutagenesis. Bioresource Technology. 2013;136:360-367. doi.org/10.1016/j.biortech.2013.03.020
53. Hu G., Fan Y., Zhang L., Yuan C., Wang J., Li W., et al. Enhanced Lipid Productivity and Photosynthesis Efficiency in a Desmodesmus sp. Mutant Induced by Heavy Carbon Ions. PLoS ONE. 2013;8;4:e60700. doi.org/10.1371/journal.pone.0060700.
54. Li J., Pora B.L.R., Dong K., Hasjim J. Health Benefits of Docosahexaenoic Acid and its Bioavailability: a Review. Food Sci. Nutr. 2021;9:5229–5243. doi.org/10.1002/fsn3.2299.
55. Munish Puri, Adarsha Gupta, Shweta Sahni. Schizochytrium sp. Trends in Microbiology. 2023;31;8:872-873. doi.org/10.1016/j.tim.2023.01.010.
56. Yu-rong Cheng, Zhi-jie Sun, Gu-zhen Cui, Xiaojin Song, Qiu Cui. A New Strategy for Strain Improvement of Aurantiochytrium sp. Based on Heavy-Ions Mutagenesis and Synergistic Effects of Cold Stress and Inhibitors of Enoyl-ACP Reductase. Enzyme and Microbial Technology. 2016;93–94:182-190. doi.org/10.1016/j.enzmictec.2016.08.019
57. Gissibl A., Sun A., Care A., Nevalainen H., Sunna A. Bioproducts from Euglena Gracilis: Synthesis and Applications. Front. Bioeng. Biotechnol. 2019;7:108. doi.org/10.3389/fbioe.2019.00108.
58. Frédérica Feuzing, Jean Pierre Mbakidi, Luc Marchal, Sandrine Bouquillon, Eric Leroy. A Review of Paramylon Processing Routes from Microalga Biomass to Non-Derivatized and Chemically Modified Products. Carbohydrate Polymers. 2022;288:119181. doi.org/10.1016/j.carbpol.2022.119181
59. Yamada K., Suzuki H., Takeuchi T., et al. Efficient Selective Breeding of Live Oil-Rich Euglena Gracilis with Fluorescence-Activated Cell Sorting. Sci. Rep. 2016;6:26327. doi.org/10.1038/srep26327.
PDF (RUS) Full-text article (in Russian)
Conflict of interest. The authors declare no conflict of interest.
Financing. The work was performed within the framework of the state assignment of the Ministry of Science and Higher Education of the Russian Federation for the ARIADNA collaboration of the NICA complex (FEFN-2024-0002, FFRS-2024-0019 and FEFN-2024-0006).
Contribution. Article was prepared with equal participation of the authors.
Article received: 20.10.2024. Accepted for publication: 25.11.2024.