Skip to main content
Log in

Impacts of Identified Bacterium Ensifer adhaerens on Microcystis aeruginosa and Subsequent Microcystin Release

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The release of microcystin and dissolved organic matter (DOM) during algae-lysing process draws much attention. In this study, Ensifer adhaerens (bacterium r23) was screened for algicidal activity against Microcystis aeruginosa (MA). The effects of dosage (2.04 × 106, 3.90 × 106, and 7.15 × 106 CFU ml−1) and dosing modes (single, double, and quadruple treatments totaling 7.15 × 106 CFU ml−1) on the release of microcystin-LR (MC-LR) and DOM were investigated. Besides cell density, intra/extra-cellular, and total MC-LR were measured during the lysing treatment. The DOM components were analyzed by parallel factor analysis (PARAFAC). Results show that the lowest dosage (2.04 × 106 CFU ml−1) not only stimulated MA growth during the initial 4 days but also triggered the production of more toxins, resulting in higher total MC-LR than the controls on 2–16 days. The higher dosages suppressed MA growth and MC-LR production simultaneously, and the total MC-LR content was substantially lower than those of the controls during the whole experimental period. The total MC-LR for the double and quadruple treatments were lower than the controls after 30-day treatment, but still higher than the single dosage. Both intracellular and extracellular DOM (IDOM, EDOM) of MA had five components, namely tyrosine-like (C1), tryptophan-like (C2 and C3), fulvic acid-like (C4), and humic acid-like (C5) substances. C1 and C3 in the EDOM resulted from MA lysis and increased along with the treatment. C2 in the EDOM came from the nutrient broth and could be consumed by r23. C4 and C5 in the EDOM mainly resulted from the growth of r23.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alamri, S. A., & Mohamed, Z. A. (2013). Selective inhibition of toxic cyanobacteria by β-carboline-containing bacterium Bacillus flexus isolated from Saudi freshwaters. Saudi Journal of Biological Sciences, 20, 357–363.

    Article  CAS  Google Scholar 

  • An, X. L., Zhang, B. Z., Zhang, H. J., Li, Y., Zheng, W., Yu, Z. M., Fu, L. J., & Zheng, T. L. (2015). Discovery of an algicidal compound from Brevibacterium sp. BS01 and its effect on a harmful algal bloom-causing species, Alexandrium tamarense. Frontiers in Microbiology, 6, 1235.

    Article  Google Scholar 

  • Beversdorf, L. J., Miller, T. R., & Mcmahon, K. D. (2013). The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PLoS One, 8(2), e56103.

    Article  CAS  Google Scholar 

  • Buchanan, R. E., & Bergey, N. E. (1975). Bergey’s manual of meterminative bacteriology (8th eds). Williams & Wilkins company, 741–751.

  • Chen, L., Chen, J., Zhang, X. Z., & Xie, P. (2016). A review of reproductive toxicity of microcystins. Journal of Hazardous Materials, 301, 381–399.

    Article  CAS  Google Scholar 

  • Chen, Z. R., Zheng, W., Yang, L. X., Boughner, L. A., Tian, Y., Zheng, T. L., & Xu, H. (2017). Lytic and chemotactic features of the plaque-forming bacterium KD531 on Phaeodactylum tricornutum. Frontiers in Microbiology, 8, 2581.

    Article  Google Scholar 

  • Dai, H. B., Xu, J. Y., Chen, Z., Yang, C. H., Hong, W. C., & Man, H. L. (2015). Chlorination of Microcystis aeruginosa: cell lyses and incomplete degradation of bioorganic substance. Desalination and Water Treatment, 138(5), 1–9.

    Google Scholar 

  • Dittmann, E., Gugger, M., Sivonen, K., & Fewer, D. P. (2015). Natural product biosynthetic diversity and comparative genomics of the cyanobacteria. Trends in Microbiology, 23(10), 642–652.

    Article  CAS  Google Scholar 

  • Du, Y. P., Ye, J., Wu, L., Yang, C. Y., Wang, L. M., & Hu, X. J. (2017). Physiological effects and toxin release in Microcystis aeruginosa and Microcystis viridis exposed to herbicide fenoxaprop-p-ethyl. Environmental Science and Pollution Research, 24, 7752–7763.

    Article  CAS  Google Scholar 

  • Gao, Y. N., Ge, F. J., Zhang, L. P., He, Y., Lu, Z. Y., Zhang, Y. Y., Liu, B. Y., Zhou, Q. H., & Wu, Z. B. (2017). Enhanced toxicity to the cyanobacterium Microcystis aeruginosa by low-dosage repeated exposure to the allelochemical N-phenyl-1-naphthylamine. Chemosphere, 174, 732–738.

    Article  CAS  Google Scholar 

  • Guan, C. W., Guo, X. Y., Li, Y., Zhang, H. J., Lei, X. Q., Cai, G. J., Guo, J. J., Yu, Z. M., & Zheng, T. L. (2015). Photoinhibition of Phaeocystis globosa resulting from oxidative stress induced by a marine algicidal bacterium Bacillus sp. LP-10. Scientific Reports, 5, 17002.

    Article  CAS  Google Scholar 

  • Guo, X. L., Liu, X. L., Pan, J. L., & Yang, H. (2015). Synergistic algicidal effect and mechanism of two diketopiperazines produced by Chryseobacterium sp. strain GLY-1106 on the harmful bloom-forming Microcystis aeruginosa. Scientific Reports, 5, 14720.

    Article  CAS  Google Scholar 

  • Jiang, T., Chen, X. S., Wang, D. Y., Liang, J., Bai, W. Y., Zhang, C., Wang, Q. L., & Wei, S. Q. (2018). Dynamics of dissolved organic matter (DOM) in a typical inland lake of the three gorges reservoir area: fluorescent properties and their implications for dissolved mercury species. Journal of Environmental Management, 206, 418–429.

    Article  CAS  Google Scholar 

  • Kang, Y. H., Park, C. S., & Han, M. S. (2012). Pseudomonas aeruginosa UCBPP-PA14 a useful bacterium capable of lysing Microcystis aeruginosa cells and degrading microcystins. Journal of Applied Phycology, 24(6), 1517–1525.

    Article  CAS  Google Scholar 

  • Kim, Y. S., Son, H. J., & Jeong, S. Y. (2015). Isolation of an algicide from a marine bacterium and its effects against the toxic dinoflagellate Alexandrium catenella and other harmful algal bloom species. Journal of Microbiology, 53(8), 511–517.

    Article  CAS  Google Scholar 

  • Kim, B. H., Sang, M., Hwang, S. J., & Han, M. S. (2008). In situ bacterial mitigation of the toxic cyanobacterium Microcystis aeruginosa implications for biological bloom control. Limnology and Oceanography: Methods, 6(10), 513–522.

    CAS  Google Scholar 

  • Laita, L. C., Calvo, L., Bes, M. T., Fillat, M. F., & Sánchez, M. L. P. (2016). Effects of benzene and several pharmaceuticals on the growth and microcystin production in Microcystis aeruginosa PCC 7806. Limnetica, 34(1), 237–246.

    Google Scholar 

  • Lezcano, M. Á., Quesada, A., & El-Shehawy, R. (2018). Seasonal dynamics of microcystin-degrading bacteria and toxic cyanobacterial blooms: Interaction and influence of abiotic factors. Harmful Algae, 71, 19–28.

    Article  CAS  Google Scholar 

  • Li, H., Ai, H. N., Kang, L., Sun, X. F., & He, Q. (2016a). Simultaneous Microcystis algicidal and microcystin degrading capability by a single Acinetobacter bacterial strain. Environmental Science & Technology, 50(21), 11903–11911.

    Article  CAS  Google Scholar 

  • Li, J. M., Li, R. H., & Li, J. (2017). Current research scenario for microcystins biodegradation - a review on fundamental knowledge, application prospects and challenges. Science of the Total Environment, 595, 615–632.

    Article  CAS  Google Scholar 

  • Li, Y., Lei, X. Q., Zhu, H., Zhang, H. J., Guan, C. W., Chen, Z. R., Zheng, W., Fu, L. J., & Zheng, T. L. (2016b). Chitinase producing bacteria with direct algicidal activity on marine diatoms. Scientific Reports, 6, 21984.

    Article  CAS  Google Scholar 

  • Li, Y., Zhu, H., Lei, X. Q., Zhang, H. J., Cai, G. J., Chen, Z. R., Fu, L. J., Xu, H., & Zheng, T. L. (2015a). The death mechanism of the harmful algal bloom species Alexandrium tamarense induced by algicidal bacterium Deinococcus sp. Y35. Frontiers in Microbiology, 6, 992.

    Google Scholar 

  • Li, Z. H., Geng, M. X., & Yang, H. (2015b). Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa. Applied Microbiology and Biotechnology, 99(2), 981–990.

    Article  CAS  Google Scholar 

  • Lin, S. Q., Pan, J. L., Li, Z. H., Liu, X. L., Tan, J., & Yang, H. (2014). Characterization of an algicidal bacterium Brevundimonas J4 and chemical defense of Synechococcus sp. BN60 against bacterium J4. Harmful Algae, 37, 1–7.

    Article  CAS  Google Scholar 

  • Liu, H. B., Song, X., Guan, Y. N., Pan, D., Li, Y. H., Xu, S. Y., & Fang, Y. Y. (2017). Role of illumination intensity in microcystin development using Microcystis aeruginosa as the model algae. Environmental Science and Pollution Research, 24(29), 23261–23272.

    Article  CAS  Google Scholar 

  • Liu, Z. Z., Zhu, J. P., Li, M., Xue, Q. Q., Zeng, Y., & Wang, Z. P. (2014). Effects of freshwater bacterial siderophore on Microcystis and Anabaena. Biological Control, 78, 42–48.

    Article  Google Scholar 

  • Lopes, W. S., Buriti, J. S., Cebalos, B. S. O., Sousa, J. T., Leite, V. D., & Vieira, F. F. (2017). Removal of microcystin-LR from drinking water using a system involving oxidation and adsorption. Water, Air, & Soil Pollution, 228(9), 1–14.

    Article  CAS  Google Scholar 

  • Lu, X. H., Zhou, B., Xu, L. L., Liu, L., Wang, G. Y., Liu, X. D., & Tang, X. X. (2016). A marine algicidal Thalassospira and its active substance against the harmful algal bloom species Karenia mikimotoi. Applied Microbiology and Biotechnology, 100(11), 5131–5139.

    Article  CAS  Google Scholar 

  • Ly, Q. V., Maqbool, T., & Hur, J. (2017). Unique characteristics of algal dissolved organic matter and their association with membrane fouling behavior: a review. Environmental Science and Pollution Research, 24(12), 11192–11205.

    Article  CAS  Google Scholar 

  • Marschner, B., & Kalbitz, K. (2003). Controls of bioavailability and biodegradability of dissolved organic matter in soils. Geoderma, 113(3–4), 211–235.

    Article  CAS  Google Scholar 

  • Mattson, M. P. (2008). Hormesis defined. Ageing Research Reviews, 7(1), 1–7.

    Article  CAS  Google Scholar 

  • Meyer, N., Bigalke, A., Kaulfuß, A., & Pohnert, G. (2017). Strategies and ecological roles of algicidal bacteria. FEMS Microbiology Reviews, 41(6), 880–899.

    Article  CAS  Google Scholar 

  • Mohamed, Z. A. (2017). Macrophytes-cyanobacteria allelopathic interactions and their implications for water resources management—A review. Limnologica, 63, 122–132.

    Article  CAS  Google Scholar 

  • Mohamed, Z. A., Deyab, M. A., Abou-Dobara, M. I., El-Sayed, A. K., & El-Raghi, W. M. (2015). Occurrence of cyanobacteria and microcystin toxins in raw and treated waters of the Nile River, Egypt: implication for water treatment and human health. Environmental Science and Pollution Research, 22(15), 11716–11727.

    Article  CAS  Google Scholar 

  • Mohamed, Z. A. (2013). Allelopathic activity of the norharmane-producing cyanobacterium Synechocystis aquatilis against cyanobacteria and microalgae. Oceanological and Hydrobiological Studies, 42(1), 1–7.

    Article  Google Scholar 

  • Ou, H., Gao, N. Y., Deng, Y., Qiao, J. L., Zhang, K. J., Li, T., & Dong, L. (2011). Mechanistic studies of Microcystic aeruginosa inactivation and degradation by UV-C irradiation and chlorination with poly-synchronous analyses. Desalination, 272(1–3), 107–119.

    Article  CAS  Google Scholar 

  • Pham, T. L., & Utsumi, M. (2018). An overview of the accumulation of microcystins in aquatic ecosystems. Journal of Environmental Management, 213, 520–529.

    Article  CAS  Google Scholar 

  • Puddick, J., Prinsep, M. R., Wood, S. A., Kaufononga, S. A. F., Cary, S. C., & Hamilton, D. P. (2014). High levels of structural diversity observed in microcystins from Microcystis CAWBG11 and characterization of six new microcystin congeners. Marine Drugs, 12(11), 5372–5395.

    Article  CAS  Google Scholar 

  • Qin, Q. L., Li, Y., Zhang, Y. J., Zhou, Z. M., Zhang, W. X., Chen, X. L., Zhang, X. Y., Zhou, B. C., Wang, L., & Zhang, Y. Z. (2011). Comparative genomics reveals a deep-sea sediment-adapted life style of Pseudoalteromonas sp. SM9913. ISME Journal, 5, 274–284.

    Article  Google Scholar 

  • Shao, J., Jiang, Y., Wang, Z., Peng, L., Luo, S., Gu, J., & Li, R. (2014). Interactions between algicidal bacteria and the cyanobacterium Microcystis aeruginosa: lytic characteristics and physiological responses in the cyanobacteria. International journal of Environmental Science and Technology, 11(2), 469–476.

    Article  CAS  Google Scholar 

  • Shao, J. H., He, Y. X., Chen, A., Peng, L., Luo, S., Wu, G. Y., Zou, H. L., & Li, R. H. (2015). Interactive effects of algicidal efficiency of Bacillus sp. B50 and bacterial community on susceptibility of Microcystis aeruginosa with different growth rates. International Biodeterioration & Biodegradation, 97, 1–6.

    Article  Google Scholar 

  • Shao, J. H., Li, R. H., Lepo, J. E., & Gu, J. D. (2013). Potential for control of harmful cyanobacterial blooms using biologically derived substances: problems and prospects. Journal of Environmental Management, 125, 149–155.

    Article  Google Scholar 

  • Shen, G. Z., Qu, D., Li, K. P., & Li, M. (2017). Composition of extracellular and intracellular polymeric substances produced by Scenedesmus and Microcystis. Environmental Engineering Science, 34(12), 887–894.

    Article  CAS  Google Scholar 

  • Shimizu, T., Oda, T., Ito, H., & Imai, I. (2017). Isolation and characterization of algicidal bacteria and its effect on a musty odor-producing cyanobacterium Dolichospermum crassum in a reservoir. Water Science and Technology: Water Supply, 17(3), 792–798.

    CAS  Google Scholar 

  • Stedmon, C. A., & Bro, R. (2008). Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnology and Oceanography: Methods, 6(11), 572–579.

    CAS  Google Scholar 

  • Sun, P. F., Esquivel-Elizondo, S., Zhao, Y. H., & Wu, Y. H. (2017a). Glucose triggers the cytotoxicity of Citrobacter sp. R1 against Microcystis aeruginosa. Science of the Total Environment, 603–604, 18–25.

    Article  CAS  Google Scholar 

  • Sun, P. F., Lin, H., Wang, G., Zhang, X. M., Zhang, Q. C., & Zhao, Y. H. (2015). Wheat bran enhances the cytotoxicity of immobilized Alcaligenes aquatilis F8 against Microcystis aeruginosa. PLoS One, 10(8), e0136429.

    Article  CAS  Google Scholar 

  • Sun, R., Sun, P. F., Zhang, J. H., Esquivel-Elizondo, S., & Wu, Y. H. (2017b). Microorganisms-based methods for harmful algal blooms control: a review. Bioresource Technology, 248, 12–20.

    Article  CAS  Google Scholar 

  • Valério, E., Vasconcelos, V., & Campos, A. (2016). New insights on the mode of action of microcystins in animal cells - a review. Mini Reviews in Medicinal Chemistry, 16, 1032–1041.

    Article  CAS  Google Scholar 

  • Wang, J., Zhang, L. J., Fan, J. J., & Wen, Y. Z. (2017a). Impacts of Rac- and S-metolachlor on cyanobacterial cell integrity and release of microcystins at different nitrogen levels. Chemosphere, 181, 619–626.

    Article  CAS  Google Scholar 

  • Wang, N. Y., Wang, K., & Wang, C. (2017b). Comparison of different algicides on growth of Microcystis aeruginosa and microcystin release, as well as its removal pathway in riverways. Frontiers of Environmental Science & Engineering, 11(6), 3.

    Article  CAS  Google Scholar 

  • Wang, X., Zhao, Y., Jiang, X., Wang, Y., Li, H., Wang, L., & Liang, W. (2018). The growth and physiological activity of Microcystis aeruginosa after flocculation using modified tannin. International Biodeterioration & Biodegradation, 133, 180–186.

    Article  CAS  Google Scholar 

  • World Health Organization (WHO). (2011). Guidelines for drinking-water quality 4th Ed. Geneva, Switzerland: WHO.

    Google Scholar 

  • Wu, L. M., Wu, H. J., Chen, L. N., Xie, S. S., Zang, H. Y., Borriss, R., & Gao, X. W. (2014). Bacilysin from Bacillus amyloliquefaciens FZB42 has specific bactericidal activity against harmful algal bloom species. Applied and Environmental Microbiology, 80(24), 7512–7520.

    Article  CAS  Google Scholar 

  • Xuan, H. L., Dai, X. Z., Li, J., Zhang, X. H., Yang, C. Y., & Lo, F. (2017). A Bacillus sp. strain with antagonistic activity against Fusarium graminearum kills Microcystis aeruginosa selectively. Science of the Total Environment, 583, 214–221.

    Article  CAS  Google Scholar 

  • Yi, Y. L., Yu, X. B., Zang, C., & Wang, G. X. (2015). Growth inhibition and microcystin degradation effects of Acinetobacter guillouiae A2 on Microcystis aeruginosa. Research in Microbiology, 166(2), 93–101.

    Article  CAS  Google Scholar 

  • Yu, X. Q., Cai, G. J., Wang, H., Hu, Z., Zheng, W., Lei, X. Q., Zhu, X. Y., Chen, Y., Chen, Q. L., Din, H. Y., Tian, Y., Fu, L. J., & Zheng, T. L. (2017). Fast-growing algicidal Streptomyces sp. U3 and its potential in harmful algal bloom controls. Journal of Hazardous Materials, 341, 138–149.

    Article  CAS  Google Scholar 

  • Zhang, N., Xu, B. B., & Qi, F. (2016b). Effect of phosphate loading on the generation of extracellular organic matters of Microcystis Aeruginosa and its derived disinfection by-products. Water, Air, & Soil Pollution, 227(8), 1–12.

    Google Scholar 

  • Zhang, Q., Song, Q., Wang, C., Zhou, C. S., Lu, C., & Zhao, M. R. (2017). Effects of glufosinate on the growth of and microcystin production by Microcystis aeruginosa at environmentally relevant concentrations. Science of the Total Environment, 575, 513–518.

    Article  CAS  Google Scholar 

  • Zhang, X., Song, T., Ma, H., & Li, L. (2016a). Physiological response of Microcystis aeruginosa to the extracellular substances from an Aeromonas sp. RSC Advances, 6, 103662–103667.

    Article  CAS  Google Scholar 

  • Zhao, L., Chen, L. N., & Yin, P. H. (2014). Algicidal metabolites produced by Bacillus sp. strain B1 against Phaeocystis globosa. Journal of Industrial Microbiology & Biotechnology, 41(3), 593–599.

    Article  CAS  Google Scholar 

  • Zuo, X., Cao, Y., Gong, A., Ding, S., Zhang, T., & Wang, Y. (2016). Removal of microcystins by highly efficient photo-catalyst Bi2WO6-activated carbon under simulated light. Water, Air, & Soil Pollution, 227(4), 1–14.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank editors for revising and editing this paper. And we also thank the anonymous re-viewers for their helpful and constructive comments that improved the manuscript substantially.

Funding

This work is supported by the Chinese National Natural Science Foundation (51672028), Fundamental Research Funds for the Central Universities (2015ZCQ-HJ-02), and the Funds from Shenzhen Techand Ecology & Environment Co., LTD (THRD004).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenyan Liang.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary material

ESM 1

(DOCX 1068 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Li, H., Fan, Q. et al. Impacts of Identified Bacterium Ensifer adhaerens on Microcystis aeruginosa and Subsequent Microcystin Release. Water Air Soil Pollut 230, 63 (2019). https://doi.org/10.1007/s11270-019-4117-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-019-4117-x

Keywords

Navigation