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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front.Environ.Sci.Eng.    2014, Vol. 8 Issue (3) : 427-432    https://doi.org/10.1007/s11783-013-0566-4
RESEARCH ARTICLE
Cadmium and lead toxicity and bioaccumulation in Microcystis aeruginosa
RZYMSKI Piotr1,(),PONIEDZIALEK Barbara,NIEDZIELSKI Przemysław2,TABACZEWSKI Piotr,WIKTOROWICZ Krzysztof
Department of Biology and Environmental Protection, Poznan University of Medical Sciences, Poznan 61-848, Poland
Faculty of Chemistry, Department of Water and Soil Analysis, Adam Mickiewicz University, Poznan 61-614, Poland
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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     
Corresponding Author(s): RZYMSKI Piotr   
Issue Date: 19 May 2014
 Cite this article:   
RZYMSKI Piotr,PONIEDZIALEK Barbara,NIEDZIELSKI Przemysław, et al. Cadmium and lead toxicity and bioaccumulation in Microcystis aeruginosa[J]. Front.Environ.Sci.Eng., 2014, 8(3): 427-432.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-013-0566-4
https://academic.hep.com.cn/fese/EN/Y2014/V8/I3/427
Fig.1  Typical 2-D graph of Microcystis aeruginosa population gated for further fluorescence analyses. FSC- forward light scatter; SSC- side light scatter
Fig.2  Mean fluorescence emission in metal-affected and unaffected samples during 24 h of incubation. Asterisks represent Kruskal–Wallis comparison between different time intervals in each sample (***-p<0.001)
Fig.3  Mean chlorophyll concentrations in metal-affected and unaffected samples after 24 h of incubation. Error bars represent standard deviation. Asterisks represent Mann–Whitney U comparison between respective Cd and Pb samples (** - p<0.01; *** - p<0.001)
metalInitial concentration /(mg·L-1)% bioaccumulatedU-Mann–WhitneyTest
Cd1178.7p<0.05
Pb59.9p<0.05
Cd5583.6p<0.05p<0.05
Pb74.2
Cd101083.2p<0.05p<0.05
Pb88.1
Cd202087.3p<0.05p<0.05
Pb90.1
Tab.1  
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
doi: 10.1371/journal.pone.0016208 pmid: 21283831
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
doi: 10.1111/j.1744-7909.2007.00368.x
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
doi: 10.3390/md8051650 pmid: 20559491
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
doi: 10.1111/j.1440-1746.1995.tb01370.x pmid: 8580413
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
doi: 10.2131/jts.23.SupplementII_143 pmid: 9760452
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
pmid: 12244757
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
doi: 10.1007/s11427-011-4222-6 pmid: 22038005
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
pmid: 21565685
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
doi: 10.1093/bmb/ldg032 pmid: 14757716
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
doi: 10.1139/m86-085 pmid: 3089567
14 Küpper H, Kroneck P M. Heavy metal uptake by plants and cyanobacteria. Metal Ions in Biological Systems, 2005, 44: 97-144
pmid: 15971666
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
doi: 10.1099/00221287-111-1-1
16 Cain A, Vannela R, Woo L K. Cyanobacteria as a biosorbent for mercuric ion. Bioresource Technology, 2008, 99(14): 6578-6586
doi: 10.1016/j.biortech.2007.11.034 pmid: 18158240
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
doi: 10.1016/j.biortech.2007.10.056 pmid: 18068356
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
doi: 10.1016/j.biortech.2010.12.028 pmid: 21195608
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
doi: 10.1146/annurev.pp.29.060178.002021
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
doi: 10.1146/annurev.pp.42.060191.001525
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
doi: 10.1007/s10765-010-0852-3
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
doi: 10.1016/j.theriogenology.2011.12.009 pmid: 22365695
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
doi: 10.1002/etc.266 pmid: 20872690
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
doi: 10.1021/es2010573 pmid: 21671609
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
doi: 10.1007/s11434-012-5337-2
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