Environmental Chemistry Letters

, Volume 12, Issue 4, pp 535–541 | Cite as

Dynamics of the toxic cyanobacterial microcystin-leucine-arginine peptide in agricultural soil

  • Sylvain Corbel
  • Noureddine Bouaïcha
  • Christian MouginEmail author
Original Paper


Microcystin-leucine-arginine (MC-LR) is a cyclic heptapeptide hepatotoxin produced by cyanobacteria such as Microcystis aeruginosa. Being highly toxic, this compound is a threat to water quality, agriculture, and human and animal health. In particular, MC-LR has been frequently detected at high concentrations in surface waters. So far, the fate of MC-LR in soils is unknown. Here, we studied degradation and soil–plant transfer of 14C-radiolabelled MC-LR in an artificial system of agricultural soil and tomato seedlings. 14C-MC-LR was dissolved in water and applied by soil irrigation, one or two times with an interval of 28 days. Results show that the 14CO2 from the degradation of 14C-MC-LR amounted to 11 % of total 14C initial input; 74–80 % of 14C-MC-LR occurred in extractible fractions analysed by HPLC. Less than 14 % of 14C-MC-LR was adsorbed on soil particles. Overall, our findings evidence for the first time a high risk of toxin leaching from the soil toward groundwater.


Cyanotoxins Microcystin-LR Soil Persistence Mineralization Plant transfer 



Authors thank Virginie Grondin and Christelle Marrault for their help and technical assistances. They acknowledge Valérie Bergeaud (UMR EGC, Thivernal-Grignon, France) for performing soil combustions, and the Biochem-Env platform (UR 251 PESSAC) for measuring soil enzymatic activities. Biochem-Env is a service of the “Investment d’Avenir” infrastructure AnaEE-France, overseen by the French National Research Agency (ANR) (ANR-11-INBS-0001). This work is part of the “Investment d’Avenir” Programme overseen by the French National Research Agency (ANR) (LabEx BASC, ANR-11-LABX-0034). The departments PESSAC and ESE are members of the EcoBASC Network. The research was also supported by grants from Région Ile-de France to S. Corbel, DIM-ASTREA Program No ast110055.


  1. Bourne DG, Riddles P, Jones GJ et al (2001) Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ Toxicol 16:523–534CrossRefGoogle Scholar
  2. Chen W, Li L, Gan N, Song L (2006a) Optimization of an effective extraction procedure for the analysis of microcystins in soils and lake sediments. Environ Pollut 143:241–246CrossRefGoogle Scholar
  3. Chen W, Song L, Gan N, Li L (2006b) Sorption, degradation and mobility of microcystins in Chinese agriculture soils: risk assessment for groundwater protection. Environ Pollut 144:752–758CrossRefGoogle Scholar
  4. Chen W, Song L, Peng L et al (2008) Reduction in microcystin concentrations in large and shallow lakes: water and sediment-interface contributions. Water Res 42:763–773CrossRefGoogle Scholar
  5. Chen J, Hu LB, Zhou W et al (2010) Degradation of microcystin-LR and RR by a Stenotrophomonas sp. strain EMS isolated from Lake Taihu. China Int J Mol Sci 11:896–911CrossRefGoogle Scholar
  6. Corbel S, Mougin C, Bouaïcha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–15CrossRefGoogle Scholar
  7. Cousins IT, Bealing DJ, James HA, Sutton A (1996) Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Res 30:481–485CrossRefGoogle Scholar
  8. Craig M, Luu HA, McCready TL et al (1996) Molecular mechanisms underlying he interaction of motuporin and microcystins with type-1 and type-2A protein phosphatases. Biochem Cell Biol Biochim Biol Cell 74:569–578CrossRefGoogle Scholar
  9. De Maagd PG-J, Hendriks AJ, Seinen W, Sijm DTHM (1999) pH-Dependent hydrophobicity of the cyanobacteria toxin microcystin-LR. Water Res 33:677–680CrossRefGoogle Scholar
  10. Del Campo FF, Ouahid Y (2010) Identification of microcystins from three collection strains of Microcystis aeruginosa. Environ Pollut 158:2906–2914CrossRefGoogle Scholar
  11. Ettoumi A, El Khalloufi F, El Ghazali I, et al (2011) Bioaccumulation of cyanobacterial toxins in aquatic organisms and its consequences for public health. In: Kattel G (ed) Zooplankton and Phytoplankton: types, characteristics and ecology. Nova Science Publishers, New York, pp 1–34Google Scholar
  12. Eynard F, Mez K, Walther J-L (2000) Risk of cyanobacterial toxins in Riga waters (Latvia). Water Res 34:2979–2988CrossRefGoogle Scholar
  13. Giaramida L, Manage PM, Edwards C et al (2013) Bacterial communities’ response to microcystins exposure and nutrient availability: linking degradation capacity to community structure. Int Biodeterior Biodegrad 84:111–117CrossRefGoogle Scholar
  14. Gupta N, Bhaskar ASB, Dangi RS et al (2001) Toxin production in batch cultures of freshwater cyanobacterium Microcystis aeruginosa. Bull Environ Contam Toxicol 67:0339–0346Google Scholar
  15. Gutiérrez-Praena D, Campos A, Azevedo J et al (2014) Exposure of Lycopersicon Esculentum to microcystin-LR: effects in the leaf proteome and toxin translocation from water to leaves and fruits. Toxins 6:1837–1854CrossRefGoogle Scholar
  16. Hastie CJ, Borthwick EB, Morrison LF et al (2005) Inhibition of several protein phosphatases by a non-covalently interacting microcystin and a novel cyanobacterial peptide, nostocyclin. Biochim Biophys Acta BBA—Gen Subj 1726:187–193CrossRefGoogle Scholar
  17. Hyenstrand P, Rohrlack T, Beattie KA et al (2003) Laboratory studies of dissolved radiolabelled microcystin-LR in lake water. Water Res 37:3299–3306Google Scholar
  18. IUSS Working Group WRB (2006) World reference base for soil resources, 2nd edn, world soil resources reports, N° 103. FAO, Rome, p 128Google Scholar
  19. Jones GJ, Bourne DG, Blakeley RL, Doelle H (1994) Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria. Nat Toxins 2:228–235CrossRefGoogle Scholar
  20. Kurki-Helasmo K, Meriluoto J (1998) Microcystin uptake inhibits growth and protein phosphatase activity in mustard (Sinapis alba L.) seedlings. Toxicon 36:1921–1926CrossRefGoogle Scholar
  21. MacKintosh RW, Dalby KN, Campbell DG et al (1995) The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 1. FEBS Lett 371:236–240CrossRefGoogle Scholar
  22. Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75:6924–6928CrossRefGoogle Scholar
  23. Miller MJ, Critchley MM, Hutson J, Fallowfield HJ (2001) The adsorption of cyanobacterial hepatotoxins from water onto soil during batch experiments. Water Res 35:1461–1468CrossRefGoogle Scholar
  24. Mohamed ZA, Al Shehri AM (2009) Microcystins in groundwater wells and their accumulation in vegetable plants irrigated with contaminated waters in Saudi Arabia. J Hazard Mater 172:310–315CrossRefGoogle Scholar
  25. Morris RJ, Williams DE, Luu HA et al (2000) The adsorption of microcystin-LR by natural clay particles. Toxicon 38:303–308CrossRefGoogle Scholar
  26. Mougin C, Pericaud C, Malosse C et al (1996) Biotransformation of the insecticide lindane by the white rot Basidiomycete Phanerochaete chrysosporium. Pestic Sci 47:51–59CrossRefGoogle Scholar
  27. Nybom SMK, Dziga D, Heikkilä JE et al (2012) Characterization of microcystin-LR removal process in the presence of probiotic bacteria. Toxicon 59:171–181CrossRefGoogle Scholar
  28. OECD (2004) Test no. 312: leaching in soil columns. Organisation for Economic Co-operation and Development, ParisGoogle Scholar
  29. Pflugmacher Wiegand C, Oberemm A et al (1998) Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochim Biophys Acta 1425:527–533CrossRefGoogle Scholar
  30. Ramanan S, Tang J, Velayudhan A (2000) Isolation and preparative purification of microcystin variants. J Chromatogr A 883:103–112CrossRefGoogle Scholar
  31. Rapala J, Berg KA, Lyra C et al (2005) Paucibacter toxinivorans gen. nov., sp. nov., a bacterium that degrades cyclic cyanobacterial hepatotoxins microcystins and nodularin. Int J Syst Evol Microbiol 55:1563–1568CrossRefGoogle Scholar
  32. Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic Cyanobacteria in Water: a guide to their public health consequences, monitoring and management, E&FN Spon, London, pp 41–111 Google Scholar
  33. Tsuji K, Naito S, Kondo F et al (1994) Stability of microcystins from cyanobacteria: effect of light on decomposition and isomerization. Environ Sci Technol 28:173–177CrossRefGoogle Scholar
  34. Valdor R, Aboal M (2007) Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon 49:769–779CrossRefGoogle Scholar
  35. Wörmer L, Cirés S, Quesada A (2011) Importance of natural sedimentation in the fate of microcystins. Chemosphere 82:1141–1146CrossRefGoogle Scholar
  36. Corbel S, Mougin C, Martin-Laurent F, Crouzet O, Bru D, Nélieu S, Bouaïcha N Phytotoxicity and ecotoxicity of a cyanobacterial extract containing microcystins under realistic environmental concentrations and in a soil–plant system. Chemosphere (in revision)Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Sylvain Corbel
    • 1
  • Noureddine Bouaïcha
    • 2
  • Christian Mougin
    • 1
    Email author
  1. 1.INRAUR251 PESSACVersaillesFrance
  2. 2.Laboratoire Ecologie, Systématique et Evolution, UMR8079, Univ. Paris-Sud/CNRS/AgroParisTechUniversité Paris-SudOrsayFrance

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