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

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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.

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References

  • 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):78–87

    Google Scholar 

  • 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 181:95–105

    Article  CAS  Google Scholar 

  • 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 122:54–66

    Article  PubMed  Google Scholar 

  • Al-Ansani MA, Abdel-Moati MAR, Al-Ansari IS (2002) Causes of fish mortality along the Qatari waters (Arabian Gulf). Int J Environ Stud 59:59–71

    Article  Google Scholar 

  • Al-Maslamani I, Le Vay L, Kennedy H (2009) Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Mar Biol 156:2001–2009

    Article  Google Scholar 

  • Banack SA, Johnson HE, Cheng R, Cox PA (2007) Production of the neurotoxin BMAA by a marine cyanobacterium. Mar Drugs 5:180–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):e49043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 90:167–173

    Article  CAS  PubMed  Google Scholar 

  • 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):322–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barkay T, Gillman M, Turner RT (1997) Effects of dissolved organic carbon and salinity on bioavailability of mercury. Appl Environ Microbiol 63:4267–4271

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384

    Article  CAS  PubMed  Google Scholar 

  • 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 9:620–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • CBP (Chesapeake Bay Program) (2016) Physical characteristics. http://www.chesapeakebay.net/discover/bayecosystem/physical

  • Chatziefthimiou AD, Richer R, Rowles H, Powell JT, Metcalf JS (2014) Cyanotoxins as a potential cause of dog poisonings in desert environments. Vet Rec 174:484–485

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272

    Article  CAS  PubMed  Google Scholar 

  • Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. PNAS 100:13380–13383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102:5074–5078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10S2:109–117

    Article  Google Scholar 

  • 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

  • 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 S2:96–100

    Article  Google Scholar 

  • 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):51–58

    Article  CAS  PubMed  Google Scholar 

  • EEA (European Environment Agency) (2016) The Baltic Sea. http://www.eea.europa.eu/publications/report_2002_0524_154909/regional-seas-around-europe/page141.html

  • Etheridge SM (2010) Paralytic shellfish poisoning: seafood safety and human health perspectives. Toxicon 56:108–122

    Article  CAS  PubMed  Google Scholar 

  • FAO (2008) Irrigation on the Middle East region in figures AQUASTAT Survey. Qatar, pp. 311e323. ftp.fao.org/docrep/fao/012/i0936e/i0936e00.pdf

  • 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 

  • 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 70:179–183

    Article  CAS  PubMed  Google Scholar 

  • 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 10:54

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 61:742–9

  • 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

  • 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 468-469:457–463

    Article  CAS  PubMed  Google Scholar 

  • 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 107:9252–9257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 152:313–138

    Article  Google Scholar 

  • 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 14:202

    Article  PubMed Central  Google Scholar 

  • 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):e83406

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

  • 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

  • Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in time and space. Springer, Dordrecht, pp 651–675

    Chapter  Google Scholar 

  • Metcalf JS, Richer R, Cox PA, Codd GA (2012) Cyanotoxins in desert environments may present a risk to human health. Sci Total Environ 421-422:118–123

    Article  CAS  PubMed  Google Scholar 

  • Metcalf JS, Banack SA, Richer R, Cox PA (2015) Neurotoxic amino acids and their isomers in desert environments. J Arid Environ 112:140–144

    Article  Google Scholar 

  • 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 110:267–269

    Article  CAS  PubMed  Google Scholar 

  • 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 9:807–820

    Article  Google Scholar 

  • 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/

  • 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

  • O’Neal RM, Chen CH, Reynolds CS, Meghal SK, Koeppe RE (1968) The neurotoxicity of L-2,4-diaminobutyric acid. Biochem J 106:699–706

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 120:216–225

    Article  CAS  PubMed  Google Scholar 

  • 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 110:35–46

  • 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 58:45–50

  • 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

  • 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 78:187–190

    Article  Google Scholar 

  • Richer R, Banack SA, Metcalf JS, Cox PA (2015) The persistence of cyanobacterial toxins in desert soils. J Arid Environ 112:134–139

    Article  Google Scholar 

  • 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 9:163e172

    Article  Google Scholar 

  • Rush T, Liu X, Lobner D (2012) Synergistic toxicity of the environmental neurotoxins methylmercury and β-N-methylamino-L-alanine. NeuroReport 23:216–219

    Article  CAS  PubMed  Google Scholar 

  • 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 46:6563–6573

    Article  CAS  PubMed  Google Scholar 

  • Shi C-X, Liang R-J (1987) The limnology of a shallow lake in China. GeoJournal 14(3):319–329

    Article  Google Scholar 

  • Smith R, Purnama A, Al-Barwani HH (2007) Sensitivity of hypersaline Arabian Gulf to seawater desalination plants. Appl Math Model 31:2347–2354

    Article  Google Scholar 

  • Vega A, Bell EA (1967) α-Amino-β-methylaminopropionic acid, a new amino acid from seeds of Cycas circinalis. Phytochemistry 6(5):759–762

    Article  CAS  Google Scholar 

  • 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 25–122

  • 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 23:15–28

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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.

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Correspondence to James S. Metcalf.

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Chatziefthimiou, A.D., Deitch, E.J., Glover, W.B. et al. Analysis of Neurotoxic Amino Acids from Marine Waters, Microbial Mats, and Seafood Destined for Human Consumption in the Arabian Gulf. Neurotox Res 33, 143–152 (2018). https://doi.org/10.1007/s12640-017-9772-3

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  • DOI: https://doi.org/10.1007/s12640-017-9772-3

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