Cadmium and lead toxicity and bioaccumulation in Microcystis aeruginosa

Abstract

The growth of human population leads to intensification of agriculture and promotes, through eutrophication, development of cyanobacteria. One of the most widespread and bloom-forming species in freshwater is toxic Microcystis aeruginosa (M. aeruginosa). Combustion of fossil fuels and metallurgical processes are the main sources of heavy metals contamination in surface water including cadmium (Cd) and lead (Pb). The following study was conducted in order to determine the effect of 1–20 mg·L^-1 of Cd and Pb on photochemistry (using flow cytometry) and growth (based on chlorophyll concentration) of M. aeruginosa as well as to estimate levels of metal bioaccumulation. We have found that 1–10 mg·L^-1 of Cd and 1–5 mg·L^-1 of Pb induced continuous enhancement of chlorophyll fluorescence during 24 h of incubation. No significant degradation of chlorophyll was observed in these samples. At higher concentrations of 20 mg·L^-1 of Cd and 10–20 mg·L^-1 of Pb chlorophyll level significantly decreased and its fluorescence was quenched. M. aeruginosa demonstrated high capability of Cd and Pb bioaccumulation, proportionally to initial metal concentration. In samples with initial concentration of 20 mg·L^-1 of Cd and Pb bioaccumulation of 87.3% and 90.1% was observed, respectively. Our study demonstrates that M. aeruginosa can potentially survive in highly metals polluted environments, be a primary source of toxic metals in the food chain and consequently contribute to enhanced toxicity of heavy metals to living organisms including human.

Keywords

Microcystis aeruginosa / heavy metals / bioaccumulation / chlorophyll / flow cytometry

References

[1] Straub C, Quillardet P, Vergalli J, de Marsac N T, Humbert J F. A day in the life of Microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS ONE, 2011, 6(1): e16208

[2] Wu Z X, Gan N Q, Song L R. Genetic diversity: geographical distribution and toxin profiles of Microcystis strains (Cyanobacteria) in China. Journal of Integrative Plant Biology, 2007, 49(3): 262-269

[3] 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, 8(5): 1650-1680

[4] Rzymski P, Poniedziałek B, Karczewski J. Gastroenteritis and liver carcinogenesis induced by cyanobacterial toxins. Gastroenterologia Polska, 2011, 18(4): 159-162

[5] Yu S Z. Primary prevention of hepatocellular carcinoma. Journal of Gastroenterology and Hepatology, 1995, 10(6): 674-682

[6] Yu S Z, Chen G, Zhi X L, Li J. Primary liver cancer: natural toxins and prevention in China. The Journal of Toxicological Sciences, 1998, 23(SupplementII): 143-147

[7] Zhou L, Yu H, Chen K. Relationship between microcystin in drinking water and colorectal cancer. Biomedical and Environmental Sciences, 2002, 15(2): 166-171

[8] Li J, Peng F, Ding D, Zhang S, Li D, Zhang T. Characteristics of the phytoplankton community and bioaccumulation of heavy metals during algal blooms in Xiangjiang River (Hunan, China). Science China Life Sciences, 2011, 54(10): 931-938

[9] Huang Y, Zou L, Zhang S, Xie S. Comparison of bacterioplankton communities in three heavily polluted streams in China. Biomedical and Environmental Sciences, 2011, 24(2): 140-145

[10] Zeng J, Yang L, Chen X, Chuai X, Wu Q L. Spatial distribution and seasonal variation of heavy metals in water and sediments of Taihu Lake. Polish Journal of Environmental Studies, 2012, 21(5): 1489-1496

[11] Järup L. Hazards of heavy metal contamination. British Medical Bulletin, 2003, 68(1): 167-182

[12] Šmirjákova S, Ondrašovičová O, Kašková A, Lakticova K. The effect of cadmium and lead pollution on human and animal health. Folia Veterinaria, 2005, 49(Suppl 3): 31-32

[13] Trevors J T, Stratton G W, Gadd G M. Cadmium transport, resistance, and toxicity in bacteria, algae, and fungi. Canadian Journal of Microbiology, 1986, 32(6): 447-464

[14] Küpper H, Kroneck P M. Heavy metal uptake by plants and cyanobacteria. Metal Ions in Biological Systems, 2005, 44: 97-144

[15] Rippka R, Deruelles J, Waterbury J B, Herdman M, Stanier R Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology, 1979, 111(1): 1-61

[16] Cain A, Vannela R, Woo L K. Cyanobacteria as a biosorbent for mercuric ion. Bioresource Technology, 2008, 99(14): 6578-6586

[17] Raungsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey N W. Removal of lead (Pb²⁺) by the cyanobacterium Gloeocapsa sp. Bioresource Technology, 2008, 99(13): 5650-5658

[18] Chakraborty N, Banerjee A, Pal R. Accumulation of lead by free and immobilized cyanobacteria with special reference to accumulation factor and recovery. Bioresource Technology, 2011, 102(5): 4191-4195

[19] Lawton I, Marsalek B, Padisák J, Chorus I. Determination of Cyanobacteria in the laboratory. In: Chorus I, Bartman J, editors. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. London: E & FN Spon, 1999, 347-367

[20] Butler W L. Energy distribution in the photochemical apparatus of photosynthesis. Annual Review of Plant Physiology, 1978, 29(1): 345-378

[21] Krause G H, Weis E. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology, 1991, 42(1): 313-349

[22] Hall D O, Rao K K. Photosynthesis. Cambridge: Cambridge University Press, 1999

[23] Murata N, Takahashi S, Nishiyama Y, Allakhverdiev S I. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta, 2007, 1767(6): 414-421

[24] Dudkowiak A, Olejarz B, Łukasiewicz J, Banaszek J, Sikora J, Wiktorowicz K. Heavy metals effect on cyanobacteria Synechocystis aquatilis study using absorption, fluorescence, flow cytometry, and photothermal measurement. International Journal of Thermophysics, 2011, 32(4): 762-773

[25] Dubelaar G B J, Jonker R R. Flow cytometry as a tool for the study of phytoplankton. Scientia Marina, 2000, 64(2): 135-156

[26] Rzymski P, Langowska A, Fliszkiewicz M, Poniedziałek B, Karczewski J, Wiktorowicz K. Flow cytometry as an estimation tool for honey bee sperm viability. Theriogenology, 2012, 77(8): 1642-1647

[27] Babu N G, Sarma P A, Attitalla I H, Murthy S D S. Effect of heavy metal ions on the photosynthetic electron transport and energy transfer in the thylakoid membrane of the cyanobacterium, Spirulina platensis. Academic Journal of Plant Sciences, 2010, 3(1): 46-49

[28] Poniedziałek B, Rzymski P, Kokociński M, Burchardt L, Wiktorowicz K. Changes of Cylindrospermopsis raciborskii and Aphanizomenon flos-aquae chlorophyll fluorescence under the influence of lead. Ochrona Środowiska i Zasobów Naturalnych, 2011, 58: 513-519 (in Polish)

[29] Zeng J, Yang L, Wang W X. High sensitivity of cyanobacterium Microcystis aeruginosa to copper and the prediction of copper toxicity. Environmental Toxicology and Chemistry, 2010, 29(10): 2260-2268

[30] Wang Z, Li J, Zhao J, Xing B. Toxicity and internalization of CuO nanoparticles to prokaryotic alga Microcystis aeruginosa as affected by dissolved organic matter. Environmental Science & Technology, 2011, 45(14): 6032-6040

[31] Zeng J, Zhao D, Ji Y, Wu Q. Comparison of heavy metal accumulation by a bloom-forming cyanobacterium, Microcystis aeruginosa. Chinese Science Bulletin, 2012, 57(28-29): 3790-3797

Acknowledgements

This project was partially supported by funds from the Young Scientists Project of Poznan University of Medical Sciences (No. 502-14-04402503-50656).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg