Skip to main content
SpringerLink
Log in

Effects of garlic and diallyl trisulfide on the growth, photosynthesis, and alkaline phosphatase activity of the toxic cyanobacterium Microcystis aeruginosa

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

To identify a botanical algicide and elucidate the response of cyanobacteria to the extract from higher plants, the effects of garlic and garlic-derived diallyl trisulfide on Microcystis aeruginosa were studied. Effects were evaluated by changes in cell density, chlorophyll a, maximum effective quantum yield (Fv/Fm), effective quantum yield (YII), non-photochemical quenching (NPQ), and rapid light curves of M. aeruginosa. In addition, alkaline phosphatase activity (APA) was measured when M. aeruginosa was incubated with diallyl trisulfide. Results indicated that the inhibition by garlic and diallyl trisulfide was significant. The 120-h 50 % effective concentrations of garlic and diallyl trisulfide (EC50) were 0.75 g L−1 and 2.84 mg L−1, respectively. Moreover, the inhibitory rate increased with increasing concentration and the growth of M. aeruginosa was inhibited by 90.0 % at the highest concentrations. We also show that the response of M. aeruginosa to stress could involve both impairment of the photosynthetic center PSII and alteration of APA. For example, at high garlic concentration (2.0 g L−1), Fv/Fm significantly decreased from 0.501 to 0.084 (p < 0.05) after 120 h of exposure. Furthermore, the total APA was significantly decreased by exposure to a high diallyl trisulfide concentration after 24 h exposure. As new algal inhibitors, there are several advantages for their utilization, such as being common, cheap, non-toxic, and with high efficiency. It would be meaningful to further research on garlic as an environmentally friendly algicide.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Beato VM, Sanchez AH, de Castro A, Montano A (2012) Effect of processing and storage time on the contents of organosulfur compounds in pickled blanched garlic. J Agric Food Chem 60(13):3485–3491

    Article  CAS  Google Scholar 

  • Berman T (1970) Alkaline phosphatases and phosphorus availability in Lake Kinneret. Limnol Oceanogr 15(5):663–674

    Article  CAS  Google Scholar 

  • Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62(3):667–683

    CAS  Google Scholar 

  • Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: ‘The CyanoHABs’. Human And Ecological Risk Assessment 7(5):1393–1407

    Article  Google Scholar 

  • Codd GA (2000) Cyanobacterial toxins, the perception of water quality, and the prioritisation of eutrophication control. Ecol Eng 16(1):51–60

    Article  Google Scholar 

  • Cornelissen G, VanNoort P, Parsons JR, Govers H (1997) Temperature dependence of slow adsorption and desorption kinetics of organic compounds in sediments. Environ Sci Technol 31(2):454–460

    Article  CAS  Google Scholar 

  • Domingos P, Rubim TK, Molica R, Azevedo S, Carmichael WW (1999) First report of microcystin production by picoplanktonic cyanobacteria isolated from a northeast Brazilian drinking water supply. Environ Toxicol 14(1):31–35

    Article  CAS  Google Scholar 

  • Drabkova M, Marsalek B, Admiraal W (2007) Photodynamic therapy against cyanobacteria. Environ Toxicol 22:112–115

    Article  CAS  Google Scholar 

  • Dziga D, Suda M, Bialczyk J, Czaja-Prokop U, Lechowski Z (2007) The alteration of Microcystis aeruginosa biomass and dissolved microcystin-LR concentration following exposure to plant-producing phenols. Environ Toxicol 22(4):341–346

    Article  CAS  Google Scholar 

  • Gross EM, Erhard D, Ivanyi E (2003) Allelopathic activity of Ceratophyllum demersum L. and Najas marina ssp intermedia (Wolfgang) Casper. Hydrobiologia 506(1–3):583–589

    Article  Google Scholar 

  • Gross EM, Meyer H, Schilling G (1996) Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry 41(1):133–138

    Article  CAS  Google Scholar 

  • Gull I, Saeed M, Shaukat H, Aslam S M, Samra Z Q, Athar A M (2012) Inhibitory effect of Allium sativum and Zingiber officinale extracts on clinically important drug resistant pathogenic bacteria. Annals of Clinical Microbiology and Antimicrobials 11(8). doi:10.1186/1476-0711-11-8

  • Hehmann A, Kaya K, Watanabe MM (2002) Selective control of Microcystis using an amino acid-a laboratory assay. J Appl Phycol 14:85–89

    Article  CAS  Google Scholar 

  • Hong Y, Hu HY, Sakoda A, Sagehashi M (2009a) Isolation and characterization of antialgal allelochemicals from Arundo donax L. Aquat Toxicol 25(3):357–367

    Google Scholar 

  • Hong Y, Hu HY, Xie X, Sakoda A, Sagehashi M, Li FM (2009b) Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. Aquat Toxicol 91(3):262–269

    Article  CAS  Google Scholar 

  • Huang BQ, Ou LJ, Hong HS, Luo HW, Wang DZ (2005) Bioavailability of dissolved organic phosphorus compounds to typical harmful dinoflagellate Prorocentrum donghaiense Lu. Mar Pollut Bull 51(8–12):838–844

    Article  CAS  Google Scholar 

  • Jassby A, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21(4):540–547

    Article  CAS  Google Scholar 

  • Korner S, Nicklisch A (2002) Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. J Phycol 38(5):862–871

    Article  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kumar KS, Dahms HU, Lee JS, Kim HC, Lee WC, Shin KH (2014) Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotoxicol Environ Saf 104:51–71

    Article  Google Scholar 

  • Lee JY, Gao Y (2012) Review of the application of garlic. Allium sativum, in aquaculture, Journal of the World Aquaculture Society 43:447–458

    Article  Google Scholar 

  • Lelkova E, Rulik M, Hekera P, Dobias P, Borovickova M, Poulickova A (2008) The influence of the coagulant PAX-18 on Planktothrix agardhii bloom in a shallow eutrophic fishpond. Fottea 8:147–154

    Article  Google Scholar 

  • Liu JS, Zhang H, Yang WD, Gao J, Ke Q (2004) Studies on biquaternary ammonium salt algicide for removing red tide algae. Mar Sci Bull 6:60–65

    Article  Google Scholar 

  • Magnusson M, Heimann K, Quayle P, Negri AP (2010) Additive toxicity of herbicide mixtures and comparative sensitivity of tropical benthic microalgae. Mar Pollut Bull 60(11):1978–1987

    Article  CAS  Google Scholar 

  • Meepagala KA, Schrader KK, Wedge DE, Duke SO (2005) Algicidal and antifungal compounds from the roots of Ruta graveolens and synthesis of their analogs. Phytochemistry 66(22):2689–2695

    Article  CAS  Google Scholar 

  • Militz TA, Southgate PC, Carton AG, Hutson KS (2014) Efficacy of garlic (Allium sativum) extract applied as a therapeutic immersion treatment for Neobenedenia sp. Management in aquaculture, Journal of Fish Diseases 37:451–461

    Article  CAS  Google Scholar 

  • Mulderij G, Mooij WM, Smolders A, Van Donk E (2005) Allelopathic inhibition of phytoplankton by exudates from Stratiotes aloides. Aquatic Botany 82(4):284–296

    Article  Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64(13):3983–3998

    Article  CAS  Google Scholar 

  • Nakai S, Zou G, Okuda T, Tsai TY, Song X, Nishijima W, Okada M (2010) Anti-cyanobacterial allelopathic effects of plants used for artificial floating islands. Allelopathy Journal 26(1):113–121

    Google Scholar 

  • Qiu HM, Geng JJ, Ren HQ, Xia XM, Wang XR, Yu Y (2013) Physiological and biochemical responses of Microcystis aeruginosa to glyphosate and its Roundup@ formulation. J Hazard Mater 248:172–176

    Article  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82(3):222–237

    Article  CAS  Google Scholar 

  • Smith JL, Boyer GL, Zimba PV (2008) A review of cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture 280(1–4):5–20

    Article  CAS  Google Scholar 

  • State Environmental Protection Administration (SEPA) (2002) Water and wastewater monitoring analysis method, 4th edn. China Environmental Science Press (in Chinese), Beijing

    Google Scholar 

  • Wang ZC, Li DH, Qin HJ, Li YX (2012) An integrated method for removal of harmful cyanobacterial blooms in eutrophic lakes. Environ Pollut 160:34–41

    Article  CAS  Google Scholar 

  • Wu ZX, Gan NQ, Huang Q, Song LR (2007) Response of Microcystis to copper stress—do phenotypes of Microcystis make a difference in stress tolerance? Environ Pollut 147(2):324–330

    Article  CAS  Google Scholar 

  • Yi YL, Lei Y, Yin YB, Zhang HY, Wang GX (2012) The antialgal activity of 40 medicinal plants against Microcystis aeruginosa. Journal of Applied Phycology 24(4):847–856

    Article  CAS  Google Scholar 

  • Zhang H, Yang WD, Gao J, Liu JS (2003) Inhibition and elimination of chlorine dioxide on Phaeocystis globosa. Chin J Appl Ecol 14:1173–1176

    CAS  Google Scholar 

  • Zhou LH, Zheng TL, Chen XH, Wang X, Chen SB, Tian Y, Hong HS (2008) The inhibitory effects of garlic (Allium sativum) and diallyl trisulfide on Alexandrium tamarense and other harmful algal species. Journal of Applied Phycology 20(4):349–358

    Article  Google Scholar 

  • Zhou LH, Zheng TL, Wang X, Ye JL, Tian Y, Hong HS (2007) Effect of five Chinese traditional medicines on the biological activity of a red-tide causing alga—Alexandrium tamarense. Harmful Algae 6(3):354–360

    Article  CAS  Google Scholar 

  • Zhou SQ, Shao YS, Gao NY, Deng Y, Qiao JL, Ou HS, Deng J (2013) Effects of different algaecides on the photosynthetic capacity, cell integrity and microcystin-LR release of Microcystis aeruginosa. Science of The Total Environment 463:111–119

    Article  Google Scholar 

  • Zhu JY, Liu BY, Wang J, Gao YN, Wu ZB (2010) Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat Toxicol 98(2):196–203

    Article  CAS  Google Scholar 

  • Zou H, Pan G, Chen H, Yuan XZ (2006) Removal of cyanobacterial blooms in Taihu Lake using local soils. II Effective removal of Microcystis aeruginosa using local soils and sediments modified by chitosan Environmental Pollution 141(2):201–205

    CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by funding from the National Science and Technology Major Project for Water Pollution Control and Treatment (2012ZX07102-004). We also thank anonymous reviewers for their valuable comments.

Author information

Authors and Affiliations

  1. Department of Environmental Science and Engineering, Fudan University, 220, Handan Road, Shanghai, 200433, PR China

    Shoubing Wang, Yuanan Wang, Xiaoxue Ma & Ziran Xu

Authors
  1. Shoubing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuanan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoxue Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ziran Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shoubing Wang.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, S., Wang, Y., Ma, X. et al. Effects of garlic and diallyl trisulfide on the growth, photosynthesis, and alkaline phosphatase activity of the toxic cyanobacterium Microcystis aeruginosa . Environ Sci Pollut Res 23, 5712–5720 (2016). https://doi.org/10.1007/s11356-015-5809-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5809-4

Keywords

Search

Navigation