Free or Protein-Bound Microcystin Accumulation by Freshwater Bivalves as a Tool to Evaluate Water Contamination by Microcystin-Producing Cyanobacteria?
Source abstract
Abstract
Cyanobacterial proliferations display rapid spatiotemporal variations that can interfere in the assessment of water contamination levels by microcystins (MC), and make necessary the use of integrative tools. This study evaluates the pertinence of bivalves Anodonta anatina and Dreissena polymorpha as bioindicators of the presence of MC-producing cyanobacteria in water. Ingested MC accumulates into two fractions in bivalve tissues—the cellular free and the protein-bound fractions—both forming the total MC fraction. Mussels were exposed to the cyanobacteria Planktothrix agardhii at densities producing an equivalent of 1, 10 and 100 µg/L of intracellular MC, with the evaluation of: (i) cyanobacterial cells and MC daily intake by mussels, (ii) free and total MC kinetics in whole individuals (using all the tissues) or only in the digestive gland, during and after the exposure, (iii) bioaccumulation factors. For each species, the kinetics of the two accumulation fractions were compared to evaluate which one best reflect levels and dynamics of MC-producing cyanobacteria in water. Results showed that the dynamic of free MC in bivalve tissues better highlight the dynamic of intracellular MC in water. Using whole D. polymorpha may be appropriate to reveal and discriminate the water contamination levels above densities of cyanobacteria producing 1 µg MC/L. Digestive glands of A. anatina appeared more sensitive to reveal low environmental concentration, but without direct correlation with levels of water contamination. Further experimentations in situ are necessary to confirm those results in order to propose the use of freshwater bivalves for a biomonitoring of MC-producing cyanobacteria in fresh waters.
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Research context
OpenAlex topics: Aquatic Ecosystems and Phytoplankton Dynamics · Marine and coastal ecosystems · Aquatic Invertebrate Ecology and Behavior
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
UMR-I 02 INERIS-URCA-ULH SEBIO Unité Stress Environnementaux et BIOsurveillance des milieux aquatiques UFR Sciences Exactes et Naturelles Moulin de la Housse, BP 1039, 51687 Reims CEDEX 2, France
Equipe Cyanobactéries, Cyanotoxines et Environnement, UMR Molécules de Communication et Adaptation des Microorganismes (MCAM), Museum National Histoire Naturelle, CNRS, 12 rue Buffon, CP 39, 75231 Paris CEDEX 05, France
Funding
Centre National de la Recherche Scientifique · PIREN-Seine
References (69)
Show source-provided references
1. Meriluoto, J., Spoof, L., and Codd, G.A. (2016). Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis, John Wiley & Sons, Ltd.10.1002/9781119068761 ↗
2. Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls10.1007/s00248-012-0159-y ↗
3. Freshwater Harmful Algal Blooms: Toxins and Children’s Health10.1016/j.cppeds.2013.10.007 ↗
4. Impact of global warming on water toxicity: Cyanotoxins10.1016/j.cofs.2017.09.013 ↗
5. Humbert, J.-F., and Fastner, J. (2017). Ecology of Cyanobacteria. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis, John Wiley & Sons, Ltd.10.1002/9781119068761.ch2 ↗
6. Microcystin-RR: Occurrence, content in water and food and toxicological studies. A review
7. Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin10.1016/j.taap.2004.08.012 ↗
8. Organic anion-transporting polypeptide (OATP) transporter family and drug disposition10.1046/j.1365-2362.33.s2.5.x ↗
9. The SLCO (former SLC21) superfamily of transporters10.1016/j.mam.2012.10.009 ↗
10. Molecular Mechanisms of Microcystin Toxicity in Animal Cells10.3390/ijms11010268 ↗
11. The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase 110.1016/0014-5793(95)00888-G ↗
12. Molecular mechanisms underlying the interaction of motuporin and microycystins with type-1 and type-2A protein phosphatases10.1139/o96-061 ↗
13. The phosphoprotein phosphatase family of Ser/Thr phosphatases as principal targets of naturally occurring toxins10.3109/10408444.2010.515564 ↗
14. Toxins of cyanobacteria10.1002/mnfr.200600185 ↗
15. Influence of sampling strategies on the monitoring of cyanobacteria in shallow lakes: Lessons from a case study in France10.1016/j.watres.2010.10.011 ↗
16. Hu, C., and Rzymski, P. (2019). Programmed Cell Death-Like and Accompanying Release of Microcystin in Freshwater Bloom-Forming Cyanobacterium Microcystis: From Identification to Ecological Relevance. Toxins, 11.10.3390/toxins11120706 ↗
17. Diurnal changes in vertical distribution and morphology of a natural population of Planktothrix agardhii (Gom.) Anagnostidis et Komárek (Cyanobacteria)
18. Horizontal migration of algal patches associated with cyanobacterial blooms in an eutrophic shallow lake10.1016/j.ecoleng.2015.12.017 ↗
19. Occurrence and elimination of cyanobacterial toxins in two Australian drinking water treatment plants10.1016/j.toxicon.2004.02.019 ↗
20. Chapter 17 Molluscs as bioindicators10.1016/S0927-5215(03)80147-9 ↗
21. Use of freshwater mussel Dreissena polymorpha to assess trace metal pollution in the lower River Po (Italy)10.1016/0045-6535(94)90042-6 ↗
22. Bivalve mollusks in metal pollution studies: From bioaccumulation to biomonitoring10.1016/j.chemosphere.2013.05.001 ↗
23. Lessons from a transplantation of zebra mussels into a small urban river: An integrated ecotoxicological assessment10.1002/tox.20591 ↗
24. Using the Asian clam as an indicator of microplastic pollution in freshwater ecosystems10.1016/j.envpol.2017.11.075 ↗
25. Organochlorine contaminants in freshwater mussels; occurrence, bioaccumulation pattern, spatio-temporal distribution and human health risk assessment from the tributaries of River Ravi, Pakistan10.1080/10807039.2017.1411780 ↗
26. Accumulation of human waterborne parasites by zebra mussels (Dreissena polymorpha) and Asian freshwater clams (Corbicula fluminea)10.1007/s00436-002-0729-x ↗
27. Bioaccumulation of human waterborne protozoa by zebra mussel (Dreissena polymorpha): Interest for water biomonitoring10.1016/j.watres.2013.09.017 ↗
28. Coupling a bio-accumulator organism and MALDI-TOF MS: An early warning detection system for microcystins in water bodies10.1007/s10811-017-1193-4 ↗
29. Impact of the Zebra Mussel, a Bivalve Invader10.2307/1311948 ↗
30. Horizontal and vertical movements of unionid mussels in a lowland river10.1899/0887-3593(2007)26[261:HAVMOU]2.0.CO;2 ↗
31. Conservation status of freshwater mussels in Europe: State of the art and future challenges10.1111/brv.12244 ↗
32. Lopes-Lima, M. (2016, February 12). Anodonta Anatina. Available online: http://www.iucnredlist.org/details/155667/0.
33. Functional response of Anodonta anatina feeding on a green alga and four strains of cyanobacteria, differing in shape, size and toxicity10.1007/s10750-007-0580-2 ↗
34. Grazing on microcystin-producing and microcystin-free phytoplankters by different filter-feeders: Implications for lake restoration10.1007/s00027-007-0916-z ↗
35. Size-structured vulnerability of the colonial cyanobacterium, Microcystis aeruginosa, to grazing by zebra mussels (Dreissena polymorpha)10.1111/fwb.12282 ↗
36. Impacts of microcystins on the feeding behaviour and energy balance of zebra mussels, Dreissena polymorpha: A bioenergetics approach10.1016/j.aquatox.2006.07.007 ↗
37. Seasonal dynamics of the hepatotoxic microcystins in various organs of four freshwater bivalves from the large eutrophic Lake Taihu of subtropical China and the risk to human consumption10.1002/tox.20146 ↗
38. Uptake and depuration of the heptapeptide toxin microcystin-LR in Mytilus galloprovincialis10.1016/0166-445X(94)00085-5 ↗
39. Bioaccumulation of hepatotoxins—A considerable risk in the Latvian environment10.1016/j.envpol.2014.10.024 ↗
40. Bioaccumulation of microcystins in invasive bivalves: A case study from the boreal lagoon ecosystem10.1016/j.oceano.2014.10.001 ↗
41. Assimilation and depuration of microcystin–LR by the zebra mussel, Dreissena polymorpha10.1016/j.aquatox.2004.06.004 ↗
42. Distribution of microcystins in a lake foodweb: No evidence for biomagnification10.1007/s00248-004-0014-x ↗
43. Mechanism and prediction for contamination of freshwater bivalves (Unionidae) with the cyanobacterial toxin microcystin in hypereutrophic Lake Suwa, Japan10.1002/tox.10075 ↗
44. Changes in concentrations of microcystins in rainbow trout, freshwater mussels, and cyanobacteria in Lakes Rotoiti and Rotoehu10.1002/tox.20174 ↗
45. Effects of physicochemical variables and cyanobacterial extracts on the immunoassay of microcystin-LR by two ELISA kits10.1046/j.1365-2672.2000.01141.x ↗
46. Cyanotoxins: Which detection technique for an optimum risk assessment?10.1016/j.watres.2017.04.025 ↗
47. Accumulation of free and covalently bound microcystins in tissues of Lymnaea stagnalis (Gastropoda) following toxic cyanobacteria or dissolved microcystin-LR exposure10.1016/j.envpol.2009.10.025 ↗
48. A method for micro-determination of total microcystin content in waterblooms of cyanobacteria (blue-green algae)10.1080/03067319208027567 ↗
49. Mass spectrometric screening method for microcystins in cyanobacteria10.1016/0041-0101(95)00163-8 ↗
50. Occurrence of an uncommon Planktothrix (Cyanoprokaryota, Oscillatoriales) in a deep lake south of the Alps10.2216/10-73.1 ↗
51. Interactions between cyanobacteria and Gastropods10.1016/j.aquatox.2006.06.004 ↗
52. Consumption of toxic cyanobacteria by Potamopyrgus antipodarum (Gastropoda, Prosobranchia) and consequences on life traits and microcystin accumulation10.1016/j.hal.2007.10.004 ↗
53. Using the MMPB technique to confirm microcystin concentrations in water measured by ELISA and HPLC (UV, MS, MS/MS)10.1016/j.toxicon.2015.07.332 ↗
54. Detection of free and covalently bound microcystins in animal tissues by liquid chromatography-tandem mass spectrometry10.1016/j.envpol.2009.10.023 ↗
55. Sanan, T.T. (2016, January 13). Measurement of “total” microcystins using the MMPB method, and application to HAB impacted surface waters. Proceedings of the Ohio AWWA Conference, Cincinnati, OH, USA.
56. Inhibition of several protein phosphatases by a non-covalently interacting microcystin and a novel cyanobacterial peptide, nostocyclin10.1016/j.bbagen.2005.06.005 ↗
57. Crystal Structures of Protein Phosphatase-1 Bound to Motuporin and Dihydromicrocystin-LA: Elucidation of the Mechanism of Enzyme Inhibition by Cyanobacterial Toxins10.1016/j.jmb.2005.11.019 ↗
58. Feeding behavior of the invasive bivalve Limnoperna fortunei (Dunker, 1857) under exposure to toxic cyanobacteria Microcystis aeruginosa10.1590/S1519-69842012000100005 ↗
59. Establishing mussel behavior as a biomarker in ecotoxicology10.1016/j.aquatox.2015.06.014 ↗
60. Formation, Characterization, and Toxicity of the Glutathione and Cysteine Conjugates of Toxic Heptapeptide Microcystins10.1021/tx00029a002 ↗
61. Cyanobacterial harmful algal blooms: State of the science and research needs. Proceedings of the Interagency, International Symposium on Cyanobacterial Harmful Algal Blooms (ISOC-HAB)10.1007/978-0-387-75865-7_1 ↗
62. Glutathione Transferases10.1146/annurev.pharmtox.45.120403.095857 ↗
63. Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: The first step of detoxication10.1016/S0304-4165(98)00107-X ↗
64. Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms10.1016/S0166-445X(00)00088-6 ↗
65. Multi-xenobiotic-resistance a possible explanation for the insensitivity of bivalves towards cyanobacterial toxins10.1016/j.toxicon.2008.09.005 ↗
66. Adaptation of freshwater mussels to cyanobacterial toxins: Response of the biotransformation and antioxidant enzymes10.1016/j.ecoenv.2011.11.037 ↗
67. Detection of total microcystin in fish tissues based on lemieux oxidation and recovery of 2-methyl-3-methoxy-4-phenylbutanoic acid (MMPB) by solid-phase microextraction gas chromatography-mass spectrometry (SPME-GC/MS)10.1080/03067319.2011.620703 ↗
68. Microcystin uptake and biochemical responses in the freshwater clam Corbicula leana P. Exposed to toxic and non-toxic Microcystis aeruginosa: Evidence of tolerance to cyanotoxins10.1016/j.toxrep.2015.01.012 ↗
69. Bioaccumulation and clearance of microcystins from salt water mussels, mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues10.1016/S0041-0101(97)00039-1 ↗