Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam

Abstract

We here report biomagnification (the increasing accumulation of bioactive, often deleterious molecules through higher trophic levels of a food chain) of the neurotoxic nonprotein amino acid beta-methylamino-l-alanine (BMAA) in the Guam ecosystem. Free-living cyanobacteria produce 0.3 microg/g BMAA, but produce 2-37 microg/g as symbionts in the coralloid roots of cycad trees. BMAA is concentrated in the developing reproductive tissues of the cycad Cycas micronesica, averaging 9 microg/g in the fleshy seed sarcotesta and a mean of 1,161 microg/g BMAA in the outermost seed layer. Flying foxes (Pteropus mariannus), which forage on the seeds, accumulate a mean of 3,556 microg/g BMAA. Flying foxes are a prized food item of the indigenous Chamorro people who boil them in coconut cream and eat them whole. Chamorros who die of amyotrophic lateral sclerosis/parkinsonism-dementia complex (AL-SPDC), a neurodegenerative disease with symptoms similar to amyotrophic lateral sclerosis, Parkinson's disease, and Alzheimer's disease, have an average of 6.6 microg/g BMAA in their brain tissues. The biomagnification of BMAA through the Guam ecosystem fits a classic triangle of increasing concentrations of toxic compounds up the food chain. This may explain why the incidence of ALS-PDC among the Chamorro was 50-100 times the incidence of amyotrophic lateral sclerosis elsewhere. Biomagnification of cyanobacterial BMAA may not be unique to Guam; our discovery of BMAA in the brain tissue from Alzheimer's patients from Canada suggests alternative ecological pathways for the bioaccumulation of BMAA in aquatic or terrestrial ecosystems.

Figures

Fig. 1.

Biomagnification of cyanobacterial BMAA in Guam. The widths of the arrows are proportional to the concentration of free BMAA delivered to the next higher trophic level.

Fig. 2.

C. micronesica Hill. (a) Habit in South Guam as a 4-m-tall unbranched tree. (b) Positively geotropic coralloid roots with tips cut to show zone of cyanobacterial invasion. (c) Cross section of coralloid root showing green ring of cyanobacterial growth. (d) P. mariannus feeding on fleshy sarcotesta of seed (photo courtesy of Merlin Tuttle, Bat Conservation International). (e) Cyanobacteria of the genus Nostoc cultured from the coralloid roots.

Fig. 3.

Representative chromatogram depicting BMAA in the frontal superior gyrus tissue of a Canadian Alzheimer's patient; peak is consistent with BMAA peaks from cyanobacteria, cycads, flying foxes, and Chamorro ALS-PDC patients.