Preview

Povolzhskiy Journal of Ecology

Advanced search

Factors influencing the increase in the proportion of toxigenic cyanobacteria of the genus Microcystis (Chroococcales, Cyanobacteria) in water supply sources

https://doi.org/10.35885/1684-7318-2025-4-437-451

Abstract

The aim of this review is to summarize current knowledge on the factors influencing the toxigenicity of cyanobacteria of the genus Microcystis and their ability to synthesize hepatotoxic peptides known as microcystins. Environmental factors affecting the ratio of toxigenic to nontoxigenic strains in aquatic ecosystems, as well as the expression levels of genes responsible for microcystin biosynthesis, are analyzed. Particular attention is given to the roles of temperature, light intensity, eutrophication, oxidative stress, and the availability of trace elements. Methods for monitoring toxigenic populations, including molecular biological approaches such as PCR and RT-PCR, are also discussed. Understanding the environmental drivers of toxigenic Microcystis proliferation may contribute to predicting the occurrence of microcystins in drinking water sources and determining optimal sampling periods for toxin monitoring in source waters.

About the Authors

A. N. Mikerov
Saratov Hygiene Medical Research Center of the Federal Budget Scientific Institution “Federal Scientific Center for Medical and Preventive Health Risk Management Technologies”; Saratov State Medical University named after V. I. Razumovsky
Russian Federation

Anatoly N. Mikerov

1A, Unit 1 Zarechnaya St., Saratov 410022,

;112 Bolshaya Kazachya St., Saratov 410012 

 



E. I. Tikhomirova
Yuri Gagarin State Technical University of Saratov
Russian Federation

Elena I. Tikhomirova

Politekhnicheskaya St., Saratov 410054



E. M. Moiseeva
Saratov Hygiene Medical Research Center of the Federal Budget Scientific Institution “Federal Scientific Center for Medical and Preventive Health Risk Management Technologies”
Russian Federation

Elizaveta M. Moiseeva

Laboratory of Chemical and Biological Monitoring of Water Quality 

1A, Unit 1 Zarechnaya St., Saratov 410022



D. A. Kuzyanov
Saratov Hygiene Medical Research Center of the Federal Budget Scientific Institution “Federal Scientific Center for Medical and Preventive Health Risk Management Technologies”
Russian Federation

Dmitriy A. Kuzyanov

1A, Unit 1 Zarechnaya St., Saratov 410022



E. M. Telesheva
Yuri Gagarin State Technical University of Saratov
Russian Federation

Elizaveta M. Telesheva

77 Politekhnicheskaya St., Saratov 410054



References

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


Review

For citations:


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

Views: 89


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1684-7318 (Print)
ISSN 2541-8963 (Online)