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Diatoms: A Novel Source for the Neurotoxin BMAA in Aquatic Environments
Stockholm University, Faculty of Science, Department of Analytical Chemistry.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
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2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 1, e84578Article in journal (Refereed) Published
Abstract [en]

Amyotrophic lateral sclerosis (ALS) or Lou Gehrig's disease is a neurological disorder linked to environmental exposure to a non-protein amino acid, beta-N-methylamino-L-alanine (BMAA). The only organisms reported to be BMAA-producing, are cyanobacteria - prokaryotic organisms. In this study, we demonstrate that diatoms - eukaryotic organisms - also produce BMAA. Ultra-high-performance liquid chromatography coupled with tandem mass spectrometry revealed the occurrence of BMAA in six investigated axenic diatom cultures. BMAA was also detected in planktonic field samples collected on the Swedish west coast that display an overrepresentation of diatoms relative to cyanobacteria. Given the ubiquity of diatoms in aquatic environments and their central role as primary producers and the main food items of zooplankton, the use of filter and suspension feeders as livestock fodder dramatically increases the risk of human exposure to BMAA-contaminated food.

Place, publisher, year, edition, pages
2014. Vol. 9, no 1, e84578
National Category
Biological Sciences Analytical Chemistry
Research subject
Analytical Chemistry; Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-100864DOI: 10.1371/journal.pone.0084578ISI: 000329460100066OAI: oai:DiVA.org:su-100864DiVA: diva2:697833
Note

AuthorCount:8;

Available from: 2014-02-19 Created: 2014-02-17 Last updated: 2017-12-06Bibliographically approved
In thesis
1. The novel sources of the neurotoxin BMAA in aquatic environments
Open this publication in new window or tab >>The novel sources of the neurotoxin BMAA in aquatic environments
2014 (English)Licentiate thesis, comprehensive summary (Other academic)
Abstract [sv]

Neurotoxinet β -N-metylamino -L-alanin (BMAA) anses vara en potentiell miljöriskfaktor för utvecklingen av den neurodegenerativa sjukdomen amyotrofisk lateralskleros (ALS) och har en potentiell roll i flertalet andra neurodegenerativa sjukdomar. Sedan 2003, då det upptäcktes att BMAA produceras av den symbiotiska cyanobakterien Nostoc punctiforme  har flera andra BMAA producerande cyanobakteriearter identifierats. Dessa arter som representanterar alla fem de fem taxonomiska grupperna och som kan återfinnas i marina , bräckta samt sötvattensekosystem världen över .

I de två studier som presenteras visas för första gången genom analys av odlade kulturer samt i fältprover att BMAA produceras av eukaryoter tillhörande kiselalger och dinoflagellatgrupperna.  Med tanke på den allmänna utbredningen av dessa två grupper i akvatiskamiljöer, deras centrala roll som primärproducenter och som främsta föda för djurplankton , bottenlevande och filtrerande organismer , antar vi att biotillgängligheten av  BMAA torde vara högre än som tidigare spekulerats .

Portugisiska sötvattensutflödena ( Ria de Aveiro och Ria Formosa ) , som har kraftiga blomningar av phytoplankton, var de ekosystem som valdes ut för att testa hypotesen . Prover av den filtrerande hjärtmusslan ( Cerastoderma edule ) från båda vattendragen visade på förekomst av BMAA i mängder som var direkt korrelerade med förekomsten utav den mest dominerande och BMAA producerande dinoflagellaten Gymnodinium catenatum , vilken  sedan tidigare är en känd  producent av Paralytic Shellfish Toxin ( PST ).

Identifieringen av dessa nya källor för BMAA tillsammans med de potentiella synergieffekter för BMAA i kombination med PST, ökar hälsorisken för allmänheten i samband med intag av BMAA kontaminerade livsmedel .

Abstract [en]

The neurotoxin, β-N-methylamino-L-alanine (BMAA) is considered to be a potential environmental risk factor for developing the neurodegenerative disease Amyotrophic Lateral Sclerosis (ALS) and have a putative role in other multiple neurodegenerative diseases. Since 2003, when it was discovered to be produced by the symbiotic cyanobacterium Nostoc punctiforme, several other cyanobacteria BMAA sources have been identified. These sources represent species from all five cyanobacteria taxonomic sections harboring marine, brackish and freshwater ecosystems worldwide.

 

In the two studies presented here, BMAA was showed for the first time to be produced by species of eukaryotes belonging to the diatom and dinoflagellate groups. This was achieved through the analysis of diatom and dinoflagellate cultures and field samples. Given the ubiquity of these two groups in aquatic environments and their central role as primary producers and as main food items for zooplankton, bottom-dwelling and filter-feeding organisms, we hypothesize that BMAA bioavailability should be higher than previously expected.

 

Portuguese transitional water bodies (Ria de Aveiro and Ria Formosa), with abundant phytoplanktonic blooms, were the selected ecosystem to test this hypothesis. Samples of the filter-feeding cockle (Cerastoderma edule) from both water bodies reveal presence of BMAA in amounts that where linked with cell abundance of the most dominant dinoflagellate, and BMAA producer Gymnodinium catenatum, a well-known Paralytic Shellfish Toxin (PST) producer.

 

The identification of novel BMAA sources together with the potential synergistic effects of BMAA with PST increased the health risk for the public in contact with BMAA-contaminated food.

Place, publisher, year, edition, pages
Stockholm University, 2014. 27 p.
Keyword
β-N-methylamino-L-alanine, diatoms, dinoflagellates, shellfish, cockles, PST
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-102998 (URN)
Presentation
2014-05-20, 540, Lilla Frescativägen 5, Stockholm, 10:10 (English)
Opponent
Supervisors
Funder
Formas
Available from: 2014-05-22 Created: 2014-04-25 Last updated: 2014-05-22Bibliographically approved
2. Mass Spectrometry of Non-protein Amino Acids: BMAA and Neurodegenerative Diseases
Open this publication in new window or tab >>Mass Spectrometry of Non-protein Amino Acids: BMAA and Neurodegenerative Diseases
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Neurodegenerative diseases have been shown to correlate positively with an ageing population. The most common neurodegenerative diseases are amyotrophic lateral sclerosis (ALS), Parkinson’s disease and Alzheimer’s disease. The cause of these diseases is believed to be the interaction between genetic and environmental factors, synergistically acting with ageing. BMAA (β-methylamino-L-alanine) is one kind of toxin present in our environment and might play an important role in the development of those diseases.

BMAA was initially isolated from cycad seeds in Guam, where the incidence of ALS/Parkinsonism-dementia complex among the indigenous people was 50 – 100 times higher than the rest of the world in the 1950’s. BMAA can induce toxic effects on rodents and primates. Furthermore, it can potentiate neuronal injury on cell cultures at concentrations as low as 10 µM. BMAA was reported to be produced by cyanobacteria, and could bio-magnify through the food chain.

In this thesis, work was initially focused on the improvement of an existing analytical method for BMAA identification and quantification using liquid chromatography coupled with tandem mass spectrometry.  Subsequently, the refined method was applied to environmental samples for probing alternative BMAA producer(s) in nature and to seafood samples for estimation of human exposure to this toxin.

In Paper I, a systematic screening of the isomers of BMAA in a database was performed and seven potential isomers were suggested. Three of them were detected or suspected in natural samples. In Paper II, a deuterated internal standard was synthesized and used for quantifying BMAA in cyanobacteria. In Paper III, Diatoms were discovered to be a BMAA producer in nature. In Paper IV, ten popular species of seafood sold in Swedish markets were screened for BMAA. Half of them were found to contain BMAA at a level of 0.01 – 0.90 µg/g wet weight. In Future perspectives, the remaining questions important in this field are raised.

Place, publisher, year, edition, pages
Stockholm: Department of Environmental Science and Analytical Chemistry, Stockholm University, 2015. 43 p.
Keyword
Neurodegenerative diseases, BMAA, Isomers, LC-MS/MS, Cyanobacteria, Diatoms, Seafood contamination
National Category
Analytical Chemistry
Research subject
Analytical Chemistry
Identifiers
urn:nbn:se:su:diva-114110 (URN)978-91-7649-028-0 (ISBN)
Public defence
2015-04-09, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrheniusväg 16 B, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2015-03-18 Created: 2015-02-20 Last updated: 2015-03-20Bibliographically approved
3. The neurotoxin β-N-methylamino-L-alanine (BMAA): Sources, bioaccumulation and extraction procedures
Open this publication in new window or tab >>The neurotoxin β-N-methylamino-L-alanine (BMAA): Sources, bioaccumulation and extraction procedures
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

β-methylamino-L-alanine (BMAA) is a neurotoxin linked to neurodegeneration, which is manifested in the devastating human diseases amyotrophic lateral sclerosis, Alzheimer’s and Parkinson’s disease. This neurotoxin is known to be produced by almost all tested species within the cyanobacterial phylum including free living as well as the symbiotic strains. The global distribution of the BMAA producers ranges from a terrestrial ecosystem on the Island of Guam in the Pacific Ocean to an aquatic ecosystem in Northern Europe, the Baltic Sea, where annually massive surface blooms occur. BMAA had been shown to accumulate in the Baltic Sea food web, with highest levels in the bottom dwelling fish-species as well as in mollusks.

One of the aims of this thesis was to test the bottom-dwelling bioaccumulation hypothesis by using a larger number of samples allowing a statistical evaluation. Hence, a large set of fish individuals from the lake Finjasjön, were caught and the BMAA concentrations in different tissues were related to the season of catching, fish gender, total weight and species. The results reveal that fish total weight and fish species were positively correlated with BMAA concentration in the fish brain. Therefore, significantly higher concentrations of BMAA in the brain were detected in plankti-benthivorous fish species and heavier (potentially older) individuals.

Another goal was to investigate the potential production of BMAA by other phytoplankton organisms. Therefore, diatom cultures were investigated and confirmed to produce BMAA, even in higher concentrations than cyanobacteria. All diatom cultures studied during this thesis work were show to contain BMAA, as well as one dinoflagellate species. This might imply that the environmental spread of BMAA in aquatic ecosystems is even higher than previously thought.

Earlier reports on the concentration of BMAA in different organisms have shown highly variable results and the methods used for quantification have been intensively discussed in the scientific community. In the most recent studies, liquid chromatography-tandem mass spectrometry (LC-MS/MS) has become the instrument of choice, due to its high sensitivity and selectivity. Even so, different studies show quite variable concentrations of BMAA. In this thesis, three of the most common BMAA extraction protocols were evaluated in order to find out if the extraction could be one of the sources of variability. It was found that the method involving precipitation of proteins using trichloroacetic acid gave the best performance, complying with all in-house validation criteria. However, extractions of diatom and cyanobacteria cultures with this validated method and quantified using LC-MS/MS still resulted in variable BMAA concentrations, which suggest that also biological reasons contribute to the discrepancies.

The current knowledge on the environmental factors that can induce or reduce BMAA production is still limited. In cyanobacteria, production of BMAA was earlier shown to be negative correlated with nitrogen availability – both in laboratory cultures as well as in natural populations. Based on this observation, it was suggested that in unicellular non-diazotrophic cyanobacteria, BMAA might take part in nitrogen metabolism. In order to find out if BMAA has a similar role in diatoms, BMAA was added to two diatom species in culture, in concentrations corresponding to those earlier found in the diatoms. The results suggest that BMAA might induce a nitrogen starvation signal in diatoms, as was earlier observed in cyanobacteria. However, diatoms recover shortly by the extracellular presence of excreted ammonia. Thus, also in diatoms, BMAA might be involved in the nitrogen balance in the cell.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2016. 69 p.
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-132142 (URN)978-91-7649-455-4 (ISBN)
External cooperation:
Public defence
2016-09-22, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council Formas
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 4: Manuscript.

Available from: 2016-08-30 Created: 2016-07-19 Last updated: 2016-08-31Bibliographically approved

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