Neurotoxicity Research

, Volume 33, Issue 1, pp 143–152 | Cite as

Analysis of Neurotoxic Amino Acids from Marine Waters, Microbial Mats, and Seafood Destined for Human Consumption in the Arabian Gulf

  • Aspassia D. Chatziefthimiou
  • Eric J. Deitch
  • William B. Glover
  • James T. Powell
  • Sandra Anne Banack
  • Renee A. Richer
  • Paul A. Cox
  • James S. Metcalf
ORIGINAL ARTICLE

Abstract

Human health risks associated with exposure to algal and cyanobacterial toxins (phycotoxins) have been largely concerned with aquatic habitats. People inhabiting desert environments may be exposed to phycotoxins present in terrestrial environments, where cyanobacterial crusts dominate. Seafood comprises a significant portion of the human diet in desert environments proximal to an ocean or sea. Consequently, in addition to terrestrial exposure to cyanotoxins, the potential exists that seafood may be an important exposure route for cyanotoxins in desert regions. Understanding the possible risk of exposure from seafood will help create cyanotoxin health guidelines for people living in environments that rely on seafood. Commonly-consumed local seafood products destined for human consumption were purchased from a fish market in Doha, Qatar. Organs were excised, extracted, and analyzed for the neurotoxic amino acid β-N-methylamino-L-alanine (BMAA) and the isomers 2,4-diaminobutyric acid (DAB) and N-2(aminoethyl)glycine (AEG). The presence and concentration of neurotoxic amino acids were investigated in organisms from various trophic levels to examine the potential for biomagnification. Although BMAA and isomers were detected in marine microbial mats, as well as in marine plankton net trawls associated with diatoms and dinoflagellates, in seafood, only AEG and DAB were present at low concentrations in various trophic levels. The findings of this study suggest that exposure to neurotoxic amino acids through seafood in the Arabian Gulf may be minor, yet the presence of BMAA in phytoplankton confirms the need for further monitoring of marine waters and seafood to protect human health.

Keywords

Seafood Seawater Microbial mats Desert BMAA and isomers Biomagnification Human consumption Risk assessment 

Notes

Acknowledgements

This publication was made possible by NPRP grant 4-775-1-116 from the Qatar National Research Fund (a member of Qatar Foundation). The statements made herein are solely the responsibility of the authors. We wish to acknowledge that Figs. 1 and 3 of this manuscript were created by Ms. Jenine Davidson. We thank Dr. Rodrigo Riera for his advice on the choice of marine species to be analyzed, and Drs. Moncef Ladjimi, Ali Sultan, Anthony Hay, and Michel Louge for providing funding and support to ADC.

References

  1. Abdul-Sahib IM (2012) Some biological aspects of the swimming crab Portunus pelagicus (Linnaeus, 1766) (Decapoda: Portunidae) in NW Arabian Gulf. J Mar Sci 27(2):78–87Google Scholar
  2. Agah H, Leermakers M, Elskens M, Faterni SMR, Baeyens W (2007) Total mercury and methylmercury concentrations in fish from the Persian Gulf and the Caspian Sea. Water Air Soil Pollut 181:95–105CrossRefGoogle Scholar
  3. Al Muftah A, Selwood AI, Foss AJ, Al-Jabri HMSJ, Potts M, Yilmaz M (2016) Algal toxins and producers in the marine waters of Qatar, Arabian Gulf. Toxicon 122:54–66CrossRefPubMedGoogle Scholar
  4. Al-Ansani MA, Abdel-Moati MAR, Al-Ansari IS (2002) Causes of fish mortality along the Qatari waters (Arabian Gulf). Int J Environ Stud 59:59–71CrossRefGoogle Scholar
  5. Al-Maslamani I, Le Vay L, Kennedy H (2009) Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Mar Biol 156:2001–2009CrossRefGoogle Scholar
  6. Banack SA, Johnson HE, Cheng R, Cox PA (2007) Production of the neurotoxin BMAA by a marine cyanobacterium. Mar Drugs 5:180–196CrossRefPubMedPubMedCentralGoogle Scholar
  7. Banack SA, Metcalf JS, Jiang L, Craighead D, Ilag LL, Cox PA (2012) Cyanobacteria produce N-(2-aminoethyl)glycine, a backbone for peptide nucleic acid which may have been the first genetic molecules for life on earth. PLoS One 7(11):e49043CrossRefPubMedPubMedCentralGoogle Scholar
  8. Banack SA, Metcalf JS, Bradley WG, Cox PA (2014) Detection of cyanobacterial neurotoxin β-N-methylamino-L-alanine within shellfish in the diet of an ALS patient in Florida. Toxicon 90:167–173CrossRefPubMedGoogle Scholar
  9. Banack SA, Caller T, Henegan P, Haney J, Murby A, Metcalf JS, Powell J, Cox PA, Stommel E (2015) Detection of cyanotoxins, beta-N-methylamino-L-alanine and microcystins, from a lake surrounded by cases of amyotrophic lateral sclerosis. Toxins 7(2):322–336CrossRefPubMedPubMedCentralGoogle Scholar
  10. Barkay T, Gillman M, Turner RT (1997) Effects of dissolved organic carbon and salinity on bioavailability of mercury. Appl Environ Microbiol 63:4267–4271PubMedPubMedCentralGoogle Scholar
  11. Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384CrossRefPubMedGoogle Scholar
  12. Brand LE, Pablo J, Compton A, Hammerschlag N, Mash DC (2010) Cyanobacterial blooms and the occurrence of the neurotoxin beta-N-methylamino-L-alanine in South Florida aquatic food webs. Harmful Algae 9:620–635CrossRefPubMedPubMedCentralGoogle Scholar
  13. CBP (Chesapeake Bay Program) (2016) Physical characteristics. http://www.chesapeakebay.net/discover/bayecosystem/physical
  14. Chatziefthimiou AD, Richer R, Rowles H, Powell JT, Metcalf JS (2014) Cyanotoxins as a potential cause of dog poisonings in desert environments. Vet Rec 174:484–485Google Scholar
  15. Chatziefthimiou AD, Metcalf JS, Glover WB, Banack SA, Dargham SR, Richer RA (2016) Cyanobacteria and cyanotoxins are present in drinking water impoundments and groundwater wells in desert environments. Toxicon 114:75–84. doi: 10.1016/j.toxicon.2016.02.016 CrossRefPubMedGoogle Scholar
  16. Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272CrossRefPubMedGoogle Scholar
  17. Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. PNAS 100:13380–13383CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa produce β-N-methylamino-L-alanine, a neurotoxic amino acid. PNAS 102:5074–5078CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cox PA, Richer R, Metcalf JS, Banack SA, Codd GA, Bradley WG (2009) Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans. Amytroph Lateral Scler 10S2:109–117CrossRefGoogle Scholar
  20. Cox PA, Davis DA, Mash DC, Metcalf JS, Banack SA (2016) Dietary exposure to an environmental toxin triggers neurofibrillary tangles and amyloid deposits in the brain. Proc R Soc B. doi: 10.1098/rspb.2015.2397
  21. Craighead D, Metcalf JS, Banack SA, Amgalan L, Reynolds HV, Batmunkh M (2009) Presence of the neurotoxic amino acids β-N-methylamino-L-alanine (BMAA) and 2,4-diaminobutyric acid (DAB) in shallow springs from the Gobi Desert. Amytroph Lateral Scler S2:96–100CrossRefGoogle Scholar
  22. Downing S, Contardo-Jara V, Pflugmacher S, Downing TG (2014) The fate of the cyanobacterial toxin β-N-methylamino-l-alanine in freshwater mussels. Ecotoxicol Environ Saf 101(1):51–58CrossRefPubMedGoogle Scholar
  23. Etheridge SM (2010) Paralytic shellfish poisoning: seafood safety and human health perspectives. Toxicon 56:108–122CrossRefPubMedGoogle Scholar
  24. FAO (2008) Irrigation on the Middle East region in figures AQUASTAT Survey. Qatar, pp. 311e323. ftp.fao.org/docrep/fao/012/i0936e/i0936e00.pdf
  25. Feulner GR, Hornby RJ (2006) Intertidal molluscs in UAE lagoons. Tribulus J Emirates Nat Hist Group 16:17–23 http://www.enhg.org/Portals/1/trib/V16N2/TribulusV16N2P17-23.pdf Google Scholar
  26. Field NC, Metcalf JS, Caller TA, Banack SA, Cox PA, Stommel EW (2013) Linking β-methylamino-L-alanine exposure to sporadic amyotrophic lateral sclerosis in Annapolis, MD. Toxicon 70:179–183CrossRefPubMedGoogle Scholar
  27. Hinder SL, Hays GC, Brooks CJ, Davies AP, Edwards M, Walne AW, Gravenor MB (2011) Toxic marine microalgae and shellfish poisoning in the British isles: history, review of epidemiology and future implications. Environ Health 10:54CrossRefPubMedPubMedCentralGoogle Scholar
  28. Horner RD, Kamins KG, Feussner JR, Grambow SC, Hoff-Lindquist J, Harati Y, Mitsumoto H, Pscuzzi R, Spencer PS, Tim R, Howard D, Smith TC, Ryan MA, Coffman CJ, Kasarkis EJ (2003) Occurrence of amyotrophic lateral sclerosis among Gulf War veterans. Neurology 61:742–9Google Scholar
  29. 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. doi: 10.1371/journal.pone.0084578
  30. 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 468-469:457–463CrossRefPubMedGoogle Scholar
  31. Jonasson S, Eriksson J, Berntzon L, Spáčil Z, Ilag LL, Ronnevi L-O, Rasmussen U, Bergman B (2010) Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggested pathways for human exposure. PNAS 107:9252–9257CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lage S, Costa PR, Moita MT, Eriksson J, Rasmussen U, Jonasson S (2014) BMAA in shellfish from two Portuguese transitional water bodies suggest the marine dinoflagellate Gymnodinium catenatum as a potential BMAA source. Aquat Toxicol 152:313–138CrossRefGoogle Scholar
  33. Li A, Song J, Hu Y, Deng L, Ding L, Li M (2016) New typical vector of neurotoxin β-N-methylamino-L-alanine (BMAA) in the marine benthic ecosystem. Mar Drugs 14:202CrossRefPubMedCentralGoogle Scholar
  34. Masseret E, Banack SA, Boumediene F, Abadie E, Brient L, Pernet F, Juntas-Morales R, Pageot N, Metcalf J, Cox PA, Camu W, the French network on BMAA/ALS (2013) Detection of BMAA in the marine environment of an ALS cluster in Southern France. PLoS One 8(12):e83406CrossRefPubMedPubMedCentralGoogle Scholar
  35. MDPS (Ministry of Development Planning and Statistics) (2013) Economic statistics report 2013 http://www.gsdp.gov.qa/portal/page/portal/GSDP_AR/knowledge_center_ar/publications/Tab7/Eco_Agriculture_Chapter_AnAb_AE_2013.pdf
  36. MDPS (Ministry of Development Planning and Statistics) (2014) Qatar information exchange environment - fish catches and exploitation rates 2000–2012. http://www.qsa.gov.qa/eng/index.htm
  37. Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in time and space. Springer, Dordrecht, pp 651–675CrossRefGoogle Scholar
  38. Metcalf JS, Richer R, Cox PA, Codd GA (2012) Cyanotoxins in desert environments may present a risk to human health. Sci Total Environ 421-422:118–123CrossRefPubMedGoogle Scholar
  39. Metcalf JS, Banack SA, Richer R, Cox PA (2015) Neurotoxic amino acids and their isomers in desert environments. J Arid Environ 112:140–144CrossRefGoogle Scholar
  40. Murch SJ, Cox PA, Banack SA, Steele JC, Cox PA (2004) Occurrence of β-methylamino-L-alanine (BMAA) in ALS/PDC patients from Guam. Acta Neurol Scand 110:267–269CrossRefPubMedGoogle Scholar
  41. Muvenna V, Dale K, Priestly B, Mueller U, Humpage A, Shaw G, Allinson G, Falconer I (2012) Health risk assessment for cyanobacterial toxins in seafood. Int J Environ Res Publ Health 9:807–820CrossRefGoogle Scholar
  42. NOAA (National Oceanic and Atmospheric Administration) (2012) Fisheries of the United States. Current fishery statistics No. 2012. http://www.st.nmfs.noaa.gov/commercial-fisheries/fus/fus12/
  43. NOAA (National Oceanic and Atmospheric Administration) (2016) Gulf of Mexico data atlas. http://www.ncddc.noaa.gov/website/DataAtlas/atlas.htm?plate=Salinity%20-%20Mean
  44. O’Neal RM, Chen CH, Reynolds CS, Meghal SK, Koeppe RE (1968) The neurotoxicity of L-2,4-diaminobutyric acid. Biochem J 106:699–706CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 120:216–225CrossRefPubMedGoogle Scholar
  46. Réveillon D, Sechet V, Hess P, Zouher A (2016a) Systematic detection of BMAA (β-N-methylamino-L-alanine) and DAB (2,4-diaminobutyric acid) in mollusks collected in shellfish production areas along the French coasts. Toxicon 110:35–46Google Scholar
  47. Réveillon D, Sechet V, Hess P, Zouher A (2016b) Production of BMAA and DAB by diatoms (Phaeodactylum tricornutum, Chaetoceros sp., Chaetoceros calcitrans and, Thalassiosira pseudonana) and bacteria isolated from a diatom culture. Harmful Algae 58:45–50Google Scholar
  48. Richer R (2009) Conservation in Qatar: impacts of increasing industrialization. Center for International and Regional Studies, Georgetown University Publication. https://repository.library.georgetown.edu/bitstream/handle/10822/558296/CIRSOccasionalPaper2ReneeRicher2009.pdf?sequence=5
  49. Richer R, Anchassi D, El-Assaad I, El-Matbouly M, Makki AF, Metcalf JS (2012) Variation in the coverage of biological crusts in the State of Qatar. J Arid Environ 78:187–190CrossRefGoogle Scholar
  50. Richer R, Banack SA, Metcalf JS, Cox PA (2015) The persistence of cyanobacterial toxins in desert soils. J Arid Environ 112:134–139CrossRefGoogle Scholar
  51. Richlen ML, Morton SL, Jamali EA, Rajan A, Anderson DM (2010) The catastrophic 2008–2009 red tide in the Arabian gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae 9:163e172CrossRefGoogle Scholar
  52. Rush T, Liu X, Lobner D (2012) Synergistic toxicity of the environmental neurotoxins methylmercury and β-N-methylamino-L-alanine. NeuroReport 23:216–219CrossRefPubMedGoogle Scholar
  53. Seubert EL, Trussell S, Eagleton J, Schnetzer A, Cetinić I, Lauri P, Jones BH, Caron DA (2012) Algal toxins and reverse osmosis desalination operations: laboratory bench testing and field monitoring of domoic acid, saxitoxin, brevetoxin and okadaic acid. Water Res 46:6563–6573CrossRefPubMedGoogle Scholar
  54. Shi C-X, Liang R-J (1987) The limnology of a shallow lake in China. GeoJournal 14(3):319–329CrossRefGoogle Scholar
  55. Smith R, Purnama A, Al-Barwani HH (2007) Sensitivity of hypersaline Arabian Gulf to seawater desalination plants. Appl Math Model 31:2347–2354CrossRefGoogle Scholar
  56. Vega A, Bell EA (1967) α-Amino-β-methylaminopropionic acid, a new amino acid from seeds of Cycas circinalis. Phytochemistry 6(5):759–762CrossRefGoogle Scholar
  57. Whitton BA (2002) Phylum Cyanophyta (cyanobacteria). In: John DM, Whitton BA, Brook AJ (eds) The freshwater algal flora of the British Isles. Cambridge University Press, Cambridge, p 25–122Google Scholar
  58. Zhang Y, Liu L, Cheng L, Cai Y, Yin H, Gao J, Gao Y (2014) Macroinverterbrate assemblages in streams and rivers of a highly developed region (Lake Taihu Basin, China). Aquat Biol 23:15–28Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Aspassia D. Chatziefthimiou
    • 1
    • 2
  • Eric J. Deitch
    • 1
  • William B. Glover
    • 3
  • James T. Powell
    • 3
  • Sandra Anne Banack
    • 3
  • Renee A. Richer
    • 2
    • 4
  • Paul A. Cox
    • 3
  • James S. Metcalf
    • 3
  1. 1.Weill Cornell Medicine - Qatar, Education CityDohaQatar
  2. 2.Richer Environments, Environmental ConsultingDohaQatar
  3. 3.Brain Chemistry LabsInstitute for EthnomedicineJacksonUSA
  4. 4.University of Wisconsin MarinetteMarinetteUSA

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