Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 16, pp 12501–12510 | Cite as

Assessment of the non-protein amino acid BMAA in Mediterranean mussel Mytilus galloprovincialis after feeding with estuarine cyanobacteria

  • Mafalda S. Baptista
  • Rita G. W. Vasconcelos
  • Paula C. Ferreira
  • C. Marisa R. Almeida
  • Vitor M. Vasconcelos
Research Article

Abstract

To determine whether 2-amino-3-methylaminopropanoic acid (BMAA) could be taken up by marine organisms from seawater or their diet mussels Mytilus galloprovincialis, collected from the North Atlantic Portuguese shore, were exposed to seawater doped with BMAA standard (for up to 48 h) or fed with cyanobacteria (for up to 15 days). Mussels were able to uptake BMAA when exposed to seawater. Mussels fed with cyanobacteria Synechocystis salina showed a rise in BMAA concentration during feeding and a decline in concentration during the subsequent depuration period. Cells from the gills and hepatopancreas of mussels fed with S. salina showed lessened metabolic activity in mussels fed for longer periods of time. A hot acidic digestion (considered to account for total BMAA) was compared with a proteolytic digestion, using pepsin, trypsin and chymotrypsin. The latter was able to extract from mussels approximately 30 % of total BMAA. Implications for BMAA trophic transfers in marine ecosystems are discussed.

Keywords

BMAA Cyanobacteria Cyanotoxins Estuaries Mussel Neurotoxins North Atlantic 

Notes

Acknowledgments

The authors wish to thank Johan Eriksson and Ralph Urbatzka for kindly providing laboratory supplies. The authors would like to acknowledge Professor Birgitta Bergman, Department of Ecology, Environment and Plant Sciences, University of Stockholm, and the European Cooperation in Science and Technology, COST Action ES 1105 “CYANOCOST-Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management” for adding value to this study through networking and knowledge sharing with European experts and researchers in the field.

This research was funded by the European Regional Development Fund (ERDF) through the project PharmAtlantic—Atlantic Area Operational Programme (Interreg IVB transnational grant 2009-1/117) and through the COMPETE—Operational Competitiveness Programme; by the Foundation for Science and Technology, Portugal (FCT) under the project “PEst-C/MAR/LA0015/2013” and the fellowship SFRH/BPD/44373/2008; and by the project MARBIOTECH (NORTE-07-0124-FEDER-000047), co-financed by the North Portugal Regional Operational Programme (ON.2 – O Novo Norte), under the National Strategic Reference Framework (NSRF), through the ERDF.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2015_4516_MOESM1_ESM.pdf (476 kb)
ESM 1 (PDF 475 kb)

References

  1. Amorim A, Vasconcelos V (1999) Dynamics of the microcystins in the mussel Mytilus galloprovincialis. Toxicon 37:1041–1052CrossRefGoogle Scholar
  2. AOAC International (2000) Official methods of analysis of AOAC International, 17th edn. In: Horwitz W (ed) Arlington, VA, USA, Association of Analytical Communities, p 2200Google Scholar
  3. Baptista MS, Cianca RCC, Lopes VR, Almeida CMR, Vasconcelos VM (2011) Determination of the non protein amino acid β-N-methylamino-L-alanine in estuarine cyanobacteria by capillary electrophoresis. Toxicon 58:410–414CrossRefGoogle Scholar
  4. Bauer E, Williams BA, Voigt C, Mosenthin R, Verstegen MWA (2003) Impact of mammalian enzyme pretreatment on the fermentability of carbohydrate-rich feedstuffs. J Sci Food Agric 83:207–214CrossRefGoogle Scholar
  5. Bell EA (2009) The discovery of BMAA, and examples of biomagnification and protein incorporation involving other non-protein amino acids. Amyotroph Lateral Scler 10(Suppl 2):21–25CrossRefGoogle Scholar
  6. Brand LE, Pablo J, Compton A, Hammerschlag N, Mash DC (2010) Cyanobacterial blooms and the occurrence of the neurotoxin beta-N-methylamino-L-alanine (BMAA) in South Florida aquatic food webs. Harmful Algae 9:620–635CrossRefGoogle Scholar
  7. Chiu AS, Gehringer MM, Braidy N, Guillermin GJ, Welch JH, Neilan BA (2013) Gliotoxicity of the cyanotoxin β-methyl-amino-L-alanine (BMAA). Scientific Reports 3: Article number 1482Google Scholar
  8. Christensen SJ, Hemscheidt TK, Trapido-Rosenthal H, Laws EA, Bidigare RR (2012) Detection and quantification of β-methylamino-L-alanine inaquatic invertebrates. Limnol Oceanogr Methods 10:891–898CrossRefGoogle Scholar
  9. Cianca RCC, Baptista MS, Lopes VRL, Vasconcelos VM (2012) The non-protein amino acid β-N-methylamino-L-alanine in Portuguese cyanobacterialisolates. Amino Acids 42:2473–2479CrossRefGoogle Scholar
  10. Cohen SA (2012) Analytical techniques for the detection of α-amino-β-methylaminopropionic acid. Analyst 137:1991–2005CrossRefGoogle Scholar
  11. Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci 100:13380–13383CrossRefGoogle Scholar
  12. Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci 102:5074–5078CrossRefGoogle Scholar
  13. Cruz-Aguado R, Winkler D, Shaw CA (2006) Lack of behavioral and neuropathological effects of dietary β-methylamino-L-alanine (BMAA) in mice. Pharmacol Biochem Behav 84:294–299CrossRefGoogle Scholar
  14. Downing S, Banack SA, Metcalf JS, Cox PA, Downing TG (2011) Nitrogen starvation of cyanobacteria results in the production of β-N-methylamino-L-alanine. Toxicon 58:187–194CrossRefGoogle Scholar
  15. Downing S, Contardo-Jara V, Pflugmacher S, Downing TD (2014) The fate of the cyanobacterial toxin β-N-methylamino-L-alanine in freshwater mussels. Ecotoxicol Environ Saf 101:51–58CrossRefGoogle Scholar
  16. Faassen EJ (2014) Presence of the neurotoxin BMAA in aquatic ecosystems: what do we really know? Toxins 6:1109–1138CrossRefGoogle Scholar
  17. Faassen EJ, Gillissen F, Lürling M (2012) A comparative study on three analytical methods for the determination of the neurotoxin BMAA in cyanobacteria. PLoS ONE 7(5):e36667CrossRefGoogle Scholar
  18. Freitas M, Azevedo J, Carvalho AP, Campos A, Vasconcelos V (2014) Effects of storage, processing and proteolytic digestion on microcystin-LR concentration in edible clams. Food Chem Toxicol 66:217–223CrossRefGoogle Scholar
  19. Glover WB, Liberto CM, McNeil WS, Banack SA, Shipley PR, Murch SJ (2012) Reactivity of β-methylamino-L-alanine in complex sample matrixes complicating detection and quantification by mass spectrometry. Anal Chem 84:7946–7953CrossRefGoogle Scholar
  20. Hur SJ, Lim BO, Decker EA, McClements DJ (2011) In vitro human digestion models for food applications. Food Chem 125:1–12CrossRefGoogle Scholar
  21. Ibelings BW, Chorus I (2007) Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–192CrossRefGoogle Scholar
  22. Jiang L, Aigret B, De Borggraeve WM, Spáčil Z, Ilag LL (2012) Selective LC-MS/MS method for the identification of BMAA from its isomers in biological samples. Anal Bioanal Chem 403:1719–1730CrossRefGoogle Scholar
  23. Jiang L, Eriksson J, Lage S, Jonasson S, Shams S, Mehine M, Ilag LL, Rasmussen U (2014) Diatoms: a novel source for the neurotoxin BMAA in aquatic environments. PLoS ONE 9(1):e84578CrossRefGoogle Scholar
  24. Jiao Y, Chen Q, Chen X, Wang X, Liao X, Jiang L, Wu J, Yang L (2014) Occurrence and transfer of a cyanobacterial neurotoxin β-methylamino-L-alanine within the aquatic food webs of Gonghu Bay (Lake Taihu, China) to evaluate the potential human health risk. Sci Total Environ 468–469:457–463CrossRefGoogle Scholar
  25. Jonasson S, Eriksson J, Berntzon L, Spáčil Z, Ilag LL, Ronnevi LO, Rasmussen U, Bergman B (2010) Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc Natl Acad Sci 107:9252–9257CrossRefGoogle Scholar
  26. Kankaanpää H, Leiniö S, Olin M, Sjövall O, Meriluoto J, Lehtonen KK (2007) Accumulation and depuration of cyanobacterial nodularin and biomarker responses in the mussel Mytilus edulis. Chemosphere 68:1210–1217CrossRefGoogle Scholar
  27. Kotai J (1972) Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research. Blindern, Oslo, Norway, Publication B-11/69, p 5Google Scholar
  28. Kubo T, Kato N, Hosoya K, Kaya K (2008) Effective determination method for a cyanobacterial neurotoxin β-N-methylamino-L-alanine. Toxicon 51:1264–1268CrossRefGoogle Scholar
  29. Li A, Tia Z, Li J, Yu R, Banack SA, Wang Z (2010) Detection of the neurotoxin BMAA within cyanobacteria isolated from freshwater in China. Toxicon 55:947–953CrossRefGoogle Scholar
  30. Li A, Fan H, Ma F, McCarron P, Thomas K, Xianghai Tang X, Quilliam MA (2012) Elucidation of matrix effects and performance of solid-phase extraction for LC-MS/MS analysis of β-N-methylamino-L-alanine (BMAA) and 2,4-diaminobutyric acid (DAB) neurotoxins in cyanobacteria. Analyst 137:1210–1219CrossRefGoogle Scholar
  31. Lobner D, Piana PMT, Salous AK, Peoples RW (2007) β-N-methylamino-L-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol Dis 25:360–366CrossRefGoogle Scholar
  32. Louzao MC, Espiña B, Cagide E, Ares IR, Alfonso A, Vieytes MR, Botana LM (2010) Cytotoxic effect of palytoxin on mussel. Toxicon 56:842–847CrossRefGoogle Scholar
  33. Lürling M, Faassen EJ, Van Eenennaam JS (2011) Effects of the cyanobacterial neurotoxin β-N-methylamino-L-alanine (BMAA) on the survival, mobility and reproduction of Daphnia magna. J Plankton Res 33:333–342CrossRefGoogle Scholar
  34. Masseret E, Banack S, Boumédiène F, Abadie E, Brient L, Pernet F, Raoul J-M, Pageot N, Metcalf J, Cox P, Camu W, the French Network on ALS clusters detection and investigation (2013) Dietary BMAA exposure in an amyotrophic lateral sclerosis cluster from southern France. PLoS ONE 8(12):e83406CrossRefGoogle Scholar
  35. Miller G (2006) Guam’s deadly stalker: on the loose worldwide? Science 28:428–431CrossRefGoogle Scholar
  36. Montine TJ, Li K, Perl DP, Galasko D (2005) Lack of β-methylamino-l-alanine in brain from controls, AD, or Chamorros with PDC. Neurology 65:768–769CrossRefGoogle Scholar
  37. Murch SJ, Cox PA, Banack SA (2004) A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc Natl Acad Sci 101:12228–12231CrossRefGoogle Scholar
  38. Osswald J, Rellán S, Gago A, Vasconcelos V (2008) Uptake and depuration of anatoxin-a by the mussel Mytilus galloprovincialis (Lamarck, 1819) under laboratory conditions. Chemosphere 72:1235–1241CrossRefGoogle Scholar
  39. Pablo J, Banack SA, Cox PA, Johnson TE, Papapetropoulos S, Bradley WG, Buck A, Mash DC (2009) Cyanobacterial neurotoxin BMAA in ALS and Alzheimer’s disease. Acta Neurol Scand 120:216–225CrossRefGoogle Scholar
  40. Pernet F, Malet N, Pastoureaud A, Vaquer A, Quéré C, Dubroca L (2012) Marine diatoms sustain growth of bivalves in a Mediterranean lagoon. J Sea Res 68:20–32CrossRefGoogle Scholar
  41. Purdie EL, Metcalf JS, Kashmiri S, Codd GA (2009) Toxicity of the cyanobacterial neurotoxin β-N-methylamino-L-alanine to three aquatic animal species. Amyotroph Lateral Scler 10(suppl 2):67–70CrossRefGoogle Scholar
  42. Riisgård HU, Larsen PS (2014) Physiologically regulated valve-closure makes mussels longterm starvation survivors: test of hypothesis. J Molluscan Stud :1–5. doi: 10.1093/mollus/eyu087
  43. Riisgård HU, Lüskow F, Pleissner D, Lundgreen K, López MAP (2013) Effect of salinity on filtration rates of mussels Mytilus edulis with special emphasis on dwarfed mussels from the low-saline Central Baltic Sea. Helgol Mar Res 67:591–598CrossRefGoogle Scholar
  44. Rosén J, Hellenäs KE (2008) Determination of the neurotoxin BMAA (β-N-methylamino-L-alanine) in cycad seed and cyanobacteria by LC-MS/MS (liquid chromatography tandem mass spectrometry). Analyst 133:1785–1789CrossRefGoogle Scholar
  45. Saker ML, Metcalf JS, Codd GA, Vasconcelos VM (2004) Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. Toxicon 43:185–194CrossRefGoogle Scholar
  46. Salomonsson ML, Hansson A, Bondesson U (2013) Development and in-house validation of a method for quantification of BMAA in mussels using dansyl chloride derivatizationand ultra performance liquid chromatography tandem mass spectrometry. Anal Methods 5:4865–4874CrossRefGoogle Scholar
  47. Santiago M, Matarredona ER, Machado A, Cano J (2006) Acute perfusion of BMAA in the rat’s striatum by in vivo microdialysis. Toxicol Lett 167:34–39CrossRefGoogle Scholar
  48. Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to public health significance, monitoring and management. E&FN Spon, London, pp 55–124Google Scholar
  49. Smith JL, Schulz KL, Zimba PV, Boyer GL (2010) Possible mechanism for the food web transfer of covalently bound microcystins. Ecotoxicol Environ Saf 73:757–761CrossRefGoogle Scholar
  50. Snyder LR, Hoggard JC, Montine TJ, Synovec RE (2010) Development and application of a comprehensive two-dimensional gas chromatography with time-of-flight mass spectrometry method for the analysis of L-β-methylamino-alanine in human tissue. J Chromatogr A 1217:4639–4647CrossRefGoogle Scholar
  51. Spáčil Z, Eriksson J, Jonasson S, Rasmussen U, Ilag LL, Bergman B (2010) Analytical protocol for identification of BMAA and DAB in biological samples. Analyst 135:127–132CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mafalda S. Baptista
    • 1
  • Rita G. W. Vasconcelos
    • 1
    • 2
  • Paula C. Ferreira
    • 1
  • C. Marisa R. Almeida
    • 1
  • Vitor M. Vasconcelos
    • 1
    • 3
  1. 1.CIMAR/CIIMAR—Interdisciplinary Centre of Marine and Environmental ResearchUniversityof PortoPortoPortugal
  2. 2.Institute of Biomedical Sciences Abel SalazarUniversityof PortoPortoPortugal
  3. 3.Department of Biology, Faculty of SciencesUniversity of PortoPortoPortugal

Personalised recommendations