Amino acid neurotoxins in feathers of the Lesser Flamingo, Phoeniconaias minor

Chemosphere

Volumn 90, Issue 2, 2013, Pages 835-839

  Metcalf, J S ^a,b,c   Banack, S A ^a   Kotut, K ^d   Krienitz, L ^e   Codd, G A ^c  

^a Institute for Ethnomedicine   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d KENYATTA UNIVERSITY   (Kenya)

^e LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

Author keywords

Amino acids; Cyanotoxins; Deposition; Lesser Flamingo; Neurotoxins

Indexed keywords

DEPOSITION; LAKES; PHASE SEPARATION; RECOVERY;

CYANOBACTERIAL TOXINS; CYANOTOXINS; DIETARY INTAKES; EAST AFRICAN RIFT; LESSER FLAMINGO; MASS MORTALITY; NEUROTOXINS; SOLID-PHASE EXTRACTION;

AMINO ACIDS;

2 AMINO 3 METHYLAMINOPROPIONIC ACID; 2,4 DIAMINOBUTYRIC ACID; AMINO ACID; ANATOXIN A; MICROCYSTIN; NEUROTOXIN;

AMINO ACID; BIOACCUMULATION; BIOGENIC MATERIAL; CYANOBACTERIUM; DIET; EXTRACTION METHOD; FEATHER; FOOD INTAKE; MASS MORTALITY; TOXIN; WADER;

ARTICLE; BIRD; CONCENTRATION (PARAMETERS); FEATHER; LIQUID CHROMATOGRAPHY; NEUROTOXICITY; NONHUMAN; PHOENICONAIAS MINOR; TANDEM MASS SPECTROMETRY;

ARTHROSPIRA; AVES; CYANOBACTERIA; PHOENICOPTERIDAE; PHOENICOPTERUS MINOR;

EID: 84869874163     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2012.09.094     Document Type: Article

References (43)

1. Banack S.A., Cox P.A. Distribution of the neurotoxic amino acid BMAA in Cycas micronesica. Bot. J. Linn. Soc. 2003, 143:165-168.
2. Banack S.A., Johnson H.E., Cheng R., Cox P.A. Production of BMAA by a marine cyanobacterium. Mar. Drugs 2007, 5:180-196.
3. Banack S.A., Murch S.J. Multiple neurotoxic items in the Chamorro diet link BMAA with ALS/PDC. Amyotrophic Lateral Scler. 2009, 10:34-40.
4. Banack S.A., Downing T.G., Spácil Z., Purdie E.L., Metcalf J.S., Downing S., Esterhuizen M., Codd G.A., Cox P.A. Distinguishing the cyanobacterial neurotoxin β-N-methylamino-l-alanine (BMAA) from its structural isomer 2,4-diaminobutyric acid (2,4-DAB). Toxicon 2010, 56:868-879.
5. Banack S.A., Metcalf J.S., Spáčil Z., Downing T.G., Downing S., Long A., Nunn P.B., Cox P.A. Distinguishing the cyanobacterial neurotoxin β-N-methylamino-l-alanine (BMAA) from other diamino acids. Toxicon 2011, 57:730-738.
6. Ballot A., Krienitz L., Kotut K., Wiegand C., Metcalf J.S., Codd G.A., Pflugmacher S. Cyanobacteria and cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya- Lakes Bogoria, Nakuru and Elmenteita. J. Plank. Res. 2004, 26:925-935.
7. Ballot A., Krienitz L., Kotut K., Wiegand C., Pflugmacher S. Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya. Harmful Algae 2005, 4:139-150.
8. Bartram S., Boland W. Chemistry and ecology of toxic birds. Chembiochem 2001, 2:809-811.
9. Best J.H., Pflugmacher S., Wiegand C., Eddy F.B., Metcalf J.S., Codd G.A. Effects of enteric bacterial and cyanobacterial lipopolysaccharides, and of microcystin-LR, on glutathione S-transferase activities in zebra fish (Danio rerio). Aquat. Toxicol. 2002, 60:223-231.
10. Carmichael W.W., Biggs D.F., Gorham P.R. Toxicology and pharmacological action of Anabaena flos-aquae toxin. Science 1975, 187:542-544.
11. Codd G.A., Bell S.G., Kaya K., Ward C.J., Beattie K.A., Metcalf J.S. Cyanobacterial toxins, exposure routes and human health. Eur. J. Phycol. 1999, 34:405-415.
12. Codd G.A., Morrison L.F., Metcalf J.S. Cyanobacterial toxins: risk management for health protection. Toxicol. Appl. Pharmacol. 2005, 203:264-272.
13. Codd G.A., Metcalf J.S., Morrison L.F., Krienitz L., Ballot A., Pflugmacher S., Wiegand C., Kotut K. Susceptibility of flamingos to cyanobacterial toxins via feeding. Vet. Rec. 2003, 152:722-723.
14. Cohen S.A. Analytical techniques for the detection of α-amino-β-methylaminopropionic acid. Analyst 2012, 137:1991-2005.
15. Cox P.A., Banack S.A., Murch S.J., Rasmussen U., Tien G., Bidigare R.R., Metcalf J.S., Morrison L.F., Codd G.A., Bergman B. Diverse taxa of cyanobacteria produce β-N-methylamino-l-alanine, a neurotoxic amino acid. Proc. Natl. Acad. Sci. USA 2005, 102:5074-5078.
16. Cox P.A., Richer R., Metcalf J.S., Banack S.A., Codd G.A., Bradley W.G. Cyanobacteria and BMAA exposure from desert dust: a possible link to sporadic ALS among Gulf War veterans. Amyotrophic Lateral Scler. 2009, 10:109-117.
17. Downing S., Banack S.A., Metcalf J.S., Cox P.A., Downing T.G. Nitrogen starvation of cyanobacteria results in the production of β-N-methylamino-l-alanine. Toxicon 2011, 58:187-194.
18. Drews G., Weckesser J. Function, structure and composition of cell walls and external layers. The Biology of Cyanobacteria 1982, 333-357. Blackwell Scientific Publications Ltd., Oxford. N.G. Carr, B.A. Whitton (Eds.).
19. Dumbacher J.P., Beehler B.M., Spande T.F., Garraffo H.M., Daly J.W. Homobatrachotoxin in the genus Pitohui: chemical defense in birds?. Science 1992, 258:799-801.
20. Dumbacher J.P., Spande T.F., Daly J.W. Batrachotoxin alkaloids from passerine birds: a second toxic bird genus (Ifrita kowaldi) from New Guinea. Proc. Natl. Acad. Sci. USA 2000, 97:12970-12975.
21. Greichus Y.A., Greichus A., Ammann B.B., Hopcraft J. Insecticides, polychlorinated biphenyls and metals in African lake ecosystems. III. Lake Nakuru, Kenya. Bull. Environ. Contam. Toxicol. 1978, 19:454-461.
22. Henriksen P., Carmichael W.W., An J., Møestrup Ø. Detection of an anatoxin-a(s)-like anticholinesterase in natural blooms and cultures of cyanobacteria/blue-green algae from Danish lakes and in the stomach contents of poisoned birds. Toxicon 1997, 35:901-913.
23. Hudnell H.K. Cyanobacterial harmful algal blooms: state of the science and research needs. Adv. Exp. Med. 2008, 619:950.
24. Koch N.D., Koch R.A., Wambua J., Kamau G.J., Mohan K.J. Mycobacterium avium-related epizootic in free-ranging lesser flamingos in Kenya. J. Wildlife Dis. 1999, 35:297-300.
25. Kotut K., Krienitz L. Does the potentially toxic cyanobacterium Microcystis exist in the soda lakes of East Africa?. Hydrobiologia 2011, 664:219-225.
26. Krienitz L., Kotut K. Fluctuating algal food populations and the occurrence of Lesser Flamingos (Phoeniconaias minor) in three Kenyan Rift Valley lakes. J. Phycol. 2010, 46:1088-1096.
27. Krienitz L., Ballot A., Kotut K., Wiegand C., Pütz S., Metcalf J.S., Codd G.A., Pflugmacher S. Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microbiol. Ecol. 2003, 43:141-148.
28. Lanaras T., Cook C.M. Toxin extraction from an Anabaenopsis milleri-dominated bloom. Sci. Total Environ. 1994, 142:163-169.
29. Lugomela C., Pratap H.B., Mgaya Y.D. Cyanobacteria blooms - a possible cause of mortality of Lesser Flamingos in Lake Manyara and Lake Big Momela, Tanzania. Harmful Algae 2006, 5:534-541.
30. Metcalf J.S., Codd G.A. Cyanotoxins. Ecology of Cyanobacteria II 2012, Springer, 802pp. B. Whitton (Ed.).
31. Lindsay J., Metcalf J.S., Codd G.A. Protection against the toxicity of microcystin-LR and cylindrospermopsin in Artemia salina and Daphnia spp. by pre-treatment with cyanobacterial lipopolysaccharide (LPS). Toxicon 2006, 48:995-1001.
32. Metcalf J.S., Morrison L.F., Krienitz L., Ballot A., Krause E., Kotut K., Pütz S., Wiegand C., Pflugmacher S., Codd G.A. Analysis of the cyanotoxins anatoxin-a and microcystins in Lesser Flamingo feathers. Toxicol. Environ. Chem. 2006, 88:159-167.
33. Metcalf J.S., Banack S.A., Lindsay J., Morrison L.F., Cox P.A., Codd G.A. Co-occurrence of β-N-methylamino-l-alanine, a neurotoxic amino acid with other cyanobacterial toxins in British waterbodies. Environ. Microbiol. 2008, 10:702-708.
34. Mohamed Z.A., Al Shehri A.M. Microcystin-producing blooms of Anabaenopsis arnoldi in a potable mountain lake in Saudi Arabia. FEMS Microbiol. Ecol. 2009, 69:98-105.
35. Murch S.J., Cox P.A., Banack S.A. A mechanism for the slow release of biomagnified cyanobacterial neurotoxins and neurodegenerative disease in Guam. Proc. Natl. Acad. Sci. USA 2004, 101:12228-12231.
36. Ndetei R., Muhandiki V.S. Mortalities of lesser flamingos in Kenyan Rift Valley saline lakes and the implication for sustainable management of the lakes. Lakes Reservoir.: Res. Manag. 2005, 10:51-58.
37. Nelson Y.M., Thampy R.J., Motelin G.K., Raini J.K., DiSante C.J., Lion L.W. Model for trace metal exposure in filter-feeding flamingos at Alkaline Rift Valley Lake, Kenya. Environ. Toxicol. Chem. 1998, 17:2302-2309.
38. O'Neal R.M., Chen C.-H., Reynolds C.S., Meghal S.K., Koeppe R.E. The 'neurotoxicity' of l-2,4-diaminobutyric acid. Biochem. J. 1968, 106:699-706.
39. Pablo J., Banack S.A., Cox P.A., Johnson T.E., Papapetropoulos S., Bradley W.G., Buck A., Mash D.C. Cyanobacterial neurotoxin BMAA in ALS and Alzheimer's disease. Acta Neurol. Scand. 2009, 120:216-225.
40. Purdie, E.L., 2010. Analysis, toxicity and occurrence of β-N-methylamino-l-alanine (BMAA), a cyanobacterial neurotoxin. PhD Thesis. University of Dundee, Dundee, UK.
41. Sipiä V.O., Neffling M.-R., Metcalf J.S., Nybom S.M.K., Meriluoto J.A.O., Codd G.A. Nodularin in feathers and livers of eiders (Somateria mollissima) caught from the western Gulf of Finland in June-September 2005. Harmful Algae 2008, 7:99-105.
42. Vareschi E. The ecology of Lake Nakuru (Kenya). I. Abundance and feeding of the Lesser Flamingo. Oecologia 1978, 32:11-35.
43. Weiss J.H., Chadwick C.W., Choi D.W. Bicarbonate dependence of glutamate receptor activation by β-N-methylamino-l-alanine: channel recording and study with related compounds. Neuron 1989, 3:321-326.