Факторы, влияющие на увеличение доли токсигенных цианобактерий рода Microcystis (Chroococcales, Cyanobacteria) в источниках водоснабжения
https://doi.org/10.35885/1684-7318-2025-4-437-451
Аннотация
Целью обзора является обобщение современных данных о факторах, влияющих на токсигенность цианобактерий рода Microcystis и синтез ими гепатотоксичных пептидов – микроцистинов. Проанализированы экологические факторы и приведены гипотезы, объясняющие их влияние на соотношение токсигенных и нетоксигенных штаммов в водоемах и экспрессию генов, ответственных за синтез микроцистина. Особое внимание уделено температуре, освещенности, эвтрофикации, окислительному стрессу и наличию микроэлементов. Приведены сведения о методах мониторинга токсигенных популяций, включая молекулярно-биологические подходы (ПЦР, ОТ-ПЦР). Исследования, посвященные изучению факторов окружающей среды, способствующих развитию токсигенных штаммов цианобактерий рода Microcystis в перспективе, могут быть использованы для прогнозирования вероятности обнаружения токсинов в воде источников хозяйственно-питьевого водоснабжения населения и определения временного интервала забора проб для определения количества микроцистина в воде водоисточника.
Ключевые слова
Об авторах
А. Н. МикеровРоссия
Микеров Анатолий Николаевич
410022, г. Саратов, ул. Заречная, здание 1А, стр. 1;
410012, г. Саратов, ул. Б. Казачья, д. 112
Е. И. Тихомирова
Россия
Тихомирова Елена Ивановна
410054, г. Саратов, ул. Политехническая, д. 77
Е. М. Моисеева
Россия
Моисеева Елизавета Михайловна
Лаборатория химико-биологического мониторинга качества воды Саратовского медицинского научного центра гигиены
410022, г. Саратов, ул. Заречная, здание 1А, стр. 1
Д. А. Кузянов
Россия
Кузянов Дмитрий Андреевич
410022, г. Саратов, ул. Заречная, здание 1А, стр. 1
Е. М. Телешева
Россия
Телешева Елизавета Михайловна
410054, г. Саратов, ул. Политехническая, д. 77
Список литературы
1. Backovic D. D., Tokodi N. Blue revolution turning green? A global concern of cyanobacteria and cyanotoxins in freshwater aquaculture: A literature review. Journal of Environmental Management, 2024, vol. 360, article no. 121115. https://doi.org/10.1016/j.jenvman.2024.121115
2. Beaver J. R., Tausz C. E., Scotese K. C., Pollard A. I., Mitchell R. M. Environmental factors influencing the quantitative distribution of microcystin and common potentially toxigenic cyanobacteria in US lakes and reservoirs. Harmful Algae, 2018, vol. 78, pp. 118–128. https://doi.org/10.1016/j.hal.2018.08.004
3. Briand E., Escoffier N., Straub C., Sabart M., Quiblier C., Humbert J. F. Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (Cyanobacteria) population. The ISME Journal, 2009, vol. 3, iss. 4, pp. 419 – 429. https://doi.org/10.1038/ismej.2008.121
4. Carmichael W. W. Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Human and Ecological Risk Assessment, 2001, vol. 7, iss. 5, pp. 1393–1407. https://doi.org/10.1080/20018091095087
5. Ceballos-Laita L., Marcuello C., Lostao A., Calvo-Begueria L., Velazquez-Campoy A., Bes M. T., Peleato M. L. Microcystin-LR binds iron, and iron promotes self-assembly. Environmental Science & Technology, 2017, vol. 51, iss. 9, pp. 4841–4850. https://doi.org/10.1021/acs.est.6b05939
6. Chen L., Gin K. Y. H., He Y. Effects of sulfate on microcystin production, photosynthesis, and oxidative stress in Microcystis aeruginosa. Environmental Science and Pollution Research, 2016, vol. 23, pp. 3586–3595. https://doi.org/10.1007/s11356-015-5605-1
7. Davis T. W., Berry D. L., Boyer G. L., Gobler C. J. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae, 2009, vol. 8, iss. 5, pp. 715–725. https://doi.org/10.1016/j.hal.2009.02.004
8. Davis T. W., Harke M. J., Marcoval M. A., Goleski J., Orano-Dawson C., Berry D. L., Gobler C. J. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquatic Microbial Ecology, 2010, vol. 61, iss. 2, pp. 149–162. https://doi.org/10.3354/ame01445
9. Dick G. J., Duhaime M. B., Evans J. T., Errera R. M., Godwin C. M., Kharbush J. J., Nitschky H. S., Powers M. A., Vanderploeg H. A., Schmidt K. C., Smith D. J., Yancey C. E., Zwiers C. C., Denef V. J. The genetic and ecophysiological diversity of Microcystis. Environmental Microbiology, 2021, vol. 23, iss. 12, pp. 7278–7313. https://doi.org/10.1111/1462-2920.15615
10. Dziallas C., Grossart H. P. Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS ONE, 2011, vol. 6, iss. 9, article no. e25569. https://doi.org/10.1371/journal.pone.0025569
11. Eldridge S. L. C., Wood T. M. Annual variations in microcystin occurrence in Upper Klamath Lake, Oregon, based on high-throughput DNA sequencing, qPCR, and environmental parameters. Lake and Reservoir Management, 2020, vol. 36, iss. 1, pp. 31–44. https://doi.org/10.1080/10402381.2019.1619112
12. Facey J. A., Apte S. C., Mitrovic S. M. A review of the effect of trace metals on freshwater cyanobacterial growth and toxin production. Toxins, 2019, vol. 11, no. 11, article no. 643. https://doi.org/10.3390/toxins11110643
13. Facey J. A., King J. J., Apte S. C., Mitrovic S. M. Assessing the importance of cobalt as a micronutrient for freshwater cyanobacteria. Journal of Phycology, 2022, vol. 58, iss. 1, pp. 71–79. https://doi.org/10.1111/jpy.13216
14. Guidelines for Drinking-Water Quality. Addendum and Vol. 2: Health Criteria and Other Supporting Information. 2nd ed. Geneva, World Health Organization, 1998. 294 p.
15. Guo Y., Meng H., Zhao S., Wang Z., Zhu L., Deng D., Liu J., He H., Xie W., Wang G., Zhang L. How does Microcystis aeruginosa respond to elevated temperature? Science of the Total Environment, 2023, vol. 889, article no. 164277. https://doi.org/10.1016/j.scitotenv.2023.164277
16. Halac S. R., Ruibal-Conti A. L., Mengo L. D. V., Ullmer F., Cativa A., Bazan R., Rodriguez M. I. Effect of iron availability on the growth and microcystin content of natural populations of Microcystis spp. from reservoirs in Central Argentina: A microcosm experiment approach. Phycology, 2023, vol. 3, no. 1, pp. 168–185. https://doi.org/10.3390/phycology3010011
17. Harris T. D., Smith V. H., Graham J. L., Van de Waal D. B., Tedesco L. P., Clercin N. Combined effects of nitrogen to phosphorus and nitrate to ammonia ratios on cyanobacterial metabolite concentrations in eutrophic Midwestern USA reservoirs. Inland Waters, 2016, vol. 6, iss. 2, pp. 199–210. https://doi.org/10.5268/IW-6.2.938
18. Hellweger F. L., Martin R. M., Eigemann F., Smith D. J., Dick G. J., Wilhelm S. W. Models predict planned phosphorus load reduction will make Lake Erie more toxic. Science, 2022, vol. 376, no. 6596, pp. 1001–1005. https://doi.org/10.1126/science.abm6791
19. Huang S., Chen Y., Wang J., Lao A., Huang H., Wang Z., Luo X., Zheng Z. Understanding the dynamics of Microcystis bloom: Unraveling the influence of suspended solids through proteomics and metabolomics approaches. Science of The Total Environment, 2024, vol. 908, article no. 168079. https://doi.org/10.1016/j.scitotenv.2023.168079
20. Kaebernick M., Neilan B. A. Ecological and molecular investigations of cyanotoxin production. FEMS Microbiology Ecology, 2001, vol. 35, iss. 1, pp. 1–9. https://doi.org/10.1111/j.1574-6941.2001.tb00782.x
21. Lahti K., Rapala J., Fardig M., Niemela M., Sivonen K. Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Water Research, 1997, vol. 31, iss. 5, pp. 1005–1012. https://doi.org/10.1016/S0043-1354(96)00353-3
22. Latour D., Perrière F., Purdie D. Higher sensitivity to hydrogen peroxide and light stress conditions of the microcystin producer Microcystis aeruginosa sp PCC7806 compared to non-producer strains. Harmful Algae, 2022, vol. 114, article no. 102219. https://doi.org/10.1016/j.hal.2022.102219
23. LeBlanc R. S., Pick F. R., Fortin N. Effect of light intensity on the relative dominance of toxigenic and nontoxigenic strains of Microcystis aeruginosa. Applied and Environmental Microbiology, 2011, vol. 77, iss. 19, pp. 7016 – 7022. https://doi.org/10.1128/AEM.05246-11
24. Li D., Kong F., Shi X., Ye L., Yu Y., Yang Z. Quantification of microcystin-producing and non-microcystin producing Microcystis populations during the 2009 and 2010 blooms in Lake Taihu using quantitative real-time PCR. Journal of Environmental Sciences, 2012, vol. 24, iss. 2, pp. 284–290. https://doi.org/10.1016/S1001-0742(11)60745-6
25. Li J., Xian X., Xiao X., Li S., Yu X. Dynamic characteristics of total and microcystinproducing Microcystis in a large deep reservoir. Environmental Pollution, 2023, vol. 335, article no. 122256. https://doi.org/10.1016/j.envpol.2023.122256
26. Li Z., An L., Yan F., Shen W., Du W., Dai R. Evaluation of the effects of different phosphorus sources on Microcystis aeruginosa growth and microcystin production via transcriptomic surveys. Water, 2023, vol. 15, no. 10, article no. 1938. https://doi.org/10.3390/w15101938
27. Lu J., Struewing I., Wymer L., Tettenhorst D. R., Shoemaker J., Allen J. Use of qPCR and RT-qPCR for monitoring variations of microcystin producers and as an early warning system to predict toxin production in an Ohio inland lake. Water Research, 2020, vol. 170, article no. 115262. https://doi.org/10.1016/j.watres.2019.115262
28. Martin R. M., Moniruzzaman M., Stark G. F., Gann E. R., Derminio D. S., Wei B., Hellweger F. L., Pinto A., Boyer G. L., Wilhelm S. W. Episodic decrease in temperature increases mcy gene transcription and cellular microcystin in continuous cultures of Microcystis aeruginosa PCC 7806. Frontiers in Microbiology, 2020, vol. 11, article no. 601864. https://doi.org/10.3389/fmicb.2020.601864
29. Molot L. A., Watson S. B., Creed I. F., Trick C. G., McCabe S. K., Verschoor M. J., Schiff S. L. A novel model for cyanobacteria bloom formation: The critical role of anoxia and ferrous iron. Freshwater Biology, 2014, vol. 59, iss. 6, pp. 1323–1340. https://doi.org/10.1111/fwb.12334
30. Ngwa F. F., Madramootoo C. A., Jabaji S. Comparison of cyanobacterial microcystin synthetase (mcy) E gene transcript levels, mcy E gene copies, and biomass as indicators of microcystin risk under laboratory and field conditions. MicrobiologyOpen, 2014, vol. 3, iss. 4, pp. 411–425. https://doi.org/10.1002/mbo3.173
31. Orr P. T., Jones G. J. Relationship between microcystin production and cell division rates in nitrogen‐limited Microcystis aeruginosa cultures. Limnology and Oceanography, 1998, vol. 43, iss. 7, pp. 1604–1614. https://doi.org/10.4319/lo.1998.43.7.1604
32. Paerl H. W., Barnard M. A. Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human-and climatically-altered world. Harmful Algae, 2020, vol. 96, article no. 101845. https://doi.org/10.1016/j.hal.2020.101845
33. Paerl H. W., Otten T. G. Blooms bite the hand that feeds them. Science, 2013, vol. 342, no. 6157, pp. 433–434. https://doi.org/10.1126/science.124527
34. Pearson L., Mihali T., Moffitt M., Kellmann R., Neilan B. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 2010, vol. 8, no. 5, pp. 1650–1680. https://doi.org/10.3390/md8051650
35. Peng G., Martin R., Dearth S., Sun X., Boyer G. L., Campagna S. Seasonally relevant cool temperatures interact with N chemistry to increase Microcystins produced in lab cultures of Microcystis aeruginosa NIES-843. Environmental Science & Technology, 2018, vol. 52, iss. 7, pp. 4127–4136. https://doi.org/10.1021/acs.est.7b06532
36. Piel T., Sandrini G., White E., Xu T., Schuurmans J. M., Huisman J., Visser P. M. Suppressing cyanobacteria with hydrogen peroxide is more effective at high light intensities. Toxins, 2019, vol. 12, no. 1, article no. 18. https://doi.org/10.3390/toxins12010018
37. Rapala J., Sivonen K., Lyra C., Niemelae S. I. Variation of Microcystins, cyanobacterial hepatotoxins, in Anabaena spp. as a function of growth stimuli. Applied and Environmental Microbiology, 1997, vol. 63, iss. 6, pp. 2206–2212. https://doi.org/10.1128/aem.63.6.2206-2212.1997
38. Rinta-Kanto J. M., Konopko E. A., DeBruyn J. M., Bourbonniere R. A., Boyer G. L. Wilhelm S. W. Lake Erie Microcystis: Relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae, 2009, vol. 8, iss. 5,pp. 665 – 673. https://doi.org/10.1016/j.hal.2008.12.004
39. Saito K., Sei Y., Miki S., Yamaguchi K. Detection of microcystin–metal complexes by using cryospray ionization-Fourier transform ion cyclotron resonance mass spectrometry. Toxicon, 2008, vol. 51, iss. 8, pp. 1496–1498. https://doi.org/10.1016/j.toxicon.2008.03.026
40. Sandrini G., Piel T., Xu T., White E., Qin H., Slot P. C., Visser P. M. Sensitivity to hydrogen peroxide of the bloom-forming cyanobacterium Microcystis PCC 7806 depends on nutrient availability. Harmful Algae, 2020, vol. 99, article no. 101916. https://doi.org/10.1016/j.hal.2020.101916
41. Sangolkar L. N., Maske S. S., Chakrabarti T. Methods for determining microcystins (peptide hepatotoxins) and microcystin-producing cyanobacteria. Water Research, 2006, vol. 40, iss. 19, pp. 3485–3496. https://doi.org/10.1016/j.watres.2006.08.010
42. Schuurmans J. M., Brinkmann B. W., Makower A. K., Dittmann E., Huisman J., Matthijs H. C. P. Microcystin interferes with defense against high oxidative stress in harmful cyanobacteria. Harmful Algae, 2018, vol. 78, pp. 47–55. https://doi.org/10.1016/j.hal.2018.07.008
43. Sevilla E., Martin-Luna B., Vela L., Bes M. T., Fillat M. F., Peleato M. L. Iron availability affects mcyD expression and microcystin‐LR synthesis in Microcystis aeruginosa PCC7806. Environmental Microbiology, 2008, vol. 10, iss. 10, pp. 247 –2483. https://doi.org/10.1111/j.1462-2920.2008.01663.x
44. Sipari H., Rantala-Ylinen A., Jokela J., Oksanen I., Sivonen K. Development of a chip assay and quantitative PCR for detecting microcystin synthetase E gene expression. Applied and Environmental Microbiology, 2010, vol. 76, iss. 12, pp. 3797–3805. https://doi.org/10.1128/AEM.00452-10
45. Stark G. F., Martin R. M., Smith L. E., Wei B., Hellweger F. L., Bullerjahn G. S., Wilhelm S. W. Microcystin aids in cold temperature acclimation: Differences between a toxic Microcystis wildtype and non-toxic mutant. Harmful Algae, 2023, vol. 129, article no. 102531. https://doi.org/10.1016/ j.hal.2023.102531
46. Svircev Z., Drobac D., Tokodi N., Mijovic B., Codd G. A., Meriluoto J. Toxicology of Microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Archives of Toxicology, 2017, vol. 91, iss. 2, pp. 621– 650. https://doi.org/10.1007/s00204-016-1921-6
47. Thomas M. K., Litchman E. Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia, 2016, vol. 763, no. 1, pp. 357 – 369. https://doi.org/10.1007/s10750-015-2390-2
48. Vaitomaa J., Rantala A., Halinen K., Rouhiainen L., Tallberg P., Mokelke L., Sivonen K. Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Applied and Environmental Microbiology, 2003, vol. 69, iss. 12, pp. 7289–7297. https://doi.org/10.1128/AEM.69.12.7289-7297.2003
49. Wang J., Chen Z., Chen H., Wen Y. Effect of hydrogen peroxide on Microcystic aeruginosa: Role of cytochromes P450. Science of the Total Environment, 2018, vol. 626, pp. 211–218. https://doi.org/10.1016/j.scitotenv.2018.01.06
50. Wang M., Shi W., Chen Q., Zhang J., Yi Q., Hu L. Effects of nutrient temporal variations on toxic genotype and microcystin concentration in two eutrophic lakes. Ecotoxicology and Environmental Safety, 2018, vol. 166, pp. 192–199. https://doi.org/10.1016/j.ecoenv.2018.09.095
51. Wei N., Song L., Gan N. Quantitative proteomic and microcystin production response of Microcystis aeruginosa to phosphorus depletion. Microorganisms, 2021, vol. 9, no. 6, article no. 1183. https://doi.org/10.3390/microorganisms9061183
52. Xu S., Zhang L., Lin K., Bai M., Wang Y., Xu M., Zhang M., Zhang C., Shi Y., Zhou H. Effects of light and water disturbance on the growth of Microcystis aeruginosa and the release of algal toxins. Water Environment Research, 2021, vol. 93, iss. 12, pp. 2958–2970. https://doi.org/10.1002/wer.1644
53. Yancey C. E., Smith D. J., Den Uyl P. A., Mohamed O. G., Yu F., Ruberg S. A., Chaffin J. D., Goodwin K. D., Tripathi A., Sherman D. H., Dick G. J. Metagenomic and metatranscriptomic insights into population diversity of Microcystis blooms: Spatial and temporal dynamics of mcy genotypes, including a partial operon that can be abundant and expressed. Applied and Environmental Microbiology, 2022, vol. 88, iss. 9, article no. e02464-21. https://doi.org/10.1128/aem.02464-21
54. Yin L., Xu L., Shi K., Chen W., Zhang Y., Wang J., Li S. Physiology, microcystin production, and transcriptomic responses of Microcystis aeruginosa exposed to calcium and magnesium. Science of The Total Environment, 2024, vol. 913, article no. 169786. https://doi.org/10.1016/j.scitotenv.2023.169786
Рецензия
Для цитирования:
Микеров А.Н., Тихомирова Е.И., Моисеева Е.М., Кузянов Д.А., Телешева Е.М. Факторы, влияющие на увеличение доли токсигенных цианобактерий рода Microcystis (Chroococcales, Cyanobacteria) в источниках водоснабжения. ПОВОЛЖСКИЙ ЭКОЛОГИЧЕСКИЙ ЖУРНАЛ. 2025;(4):437-451. https://doi.org/10.35885/1684-7318-2025-4-437-451
For citation:
Mikerov A.N., Tikhomirova E.I., Moiseeva E.M., Kuzyanov D.A., Telesheva E.M. Factors influencing the increase in the proportion of toxigenic cyanobacteria of the genus Microcystis (Chroococcales, Cyanobacteria) in water supply sources. Povolzhskiy Journal of Ecology. 2025;(4):437-451. (In Russ.) https://doi.org/10.35885/1684-7318-2025-4-437-451





































