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

Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13380-3. doi: 10.1073/pnas.2235808100.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids, Diamino / metabolism*
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Brain / metabolism
  • Chiroptera
  • Cyanobacteria / metabolism*
  • Cyanobacteria Toxins
  • Cycas / metabolism
  • Dementia / pathology
  • Ecosystem
  • Food Chain
  • Guam
  • Humans
  • Neurodegenerative Diseases / metabolism*
  • Neurotoxins / metabolism*
  • Parkinson Disease / pathology
  • Plant Roots / metabolism
  • Plant Roots / microbiology
  • Plants, Edible / microbiology

Substances

  • Amino Acids, Diamino
  • Cyanobacteria Toxins
  • Neurotoxins
  • beta-N-methylamino-L-alanine