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  • 1. Braga, Ana C.
    et al.
    Lage, Sandra
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Pacheco, Mário
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Costa, Pedro R.
    Native (Ruditapes decussatus) and non-indigenous (R. philippinarum) shellfish species living in sympatry: Comparison of regulated and non-regulated biotoxins accumulation2017In: Marine Environmental Research, ISSN 0141-1136, E-ISSN 1879-0291, Vol. 129, p. 147-155Article in journal (Refereed)
    Abstract [en]

    The native Ruditapes decussatus and the non-indigenous Ruditapes philippinarum are an important target of shellfish industries. The aim of this study was to compare an invader with a native species living in sympatry in the view of marine biotoxins accumulation. Samples were analysed for regulated and non regulated biotoxins. The consistently occurrence of okadaic acid-group toxins and BMAA, may cause human health problems and economical losses. A strong positive relationship was observed between species, with significantly higher DSP toxicity in R. decussatus. Similar toxin profiles dominated by DTX3 in both species suggests similar metabolic pathways. Lower DSP toxicity in R. philippinarum may favour their cultivation, but a tendency for higher levels of the non-regulated BMAA was observed, indicating risks for consumers that are not monitored. This study highlights the need to better understand the physiological responses and adaptations allowing similar species exposed to the same conditions to present different toxicity levels.

  • 2.
    Eriksson, Johan
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Jonasson, Sara
    Stockholm University, Faculty of Science, Department of Botany.
    Papaefthimiou, Dimitra
    Rasmussen, Ulla
    Bergman, Birgitta
    Improving derivatization efficiency of BMAA utilizing AccQ-Tag ia a complex cyanobacterial matrix2009In: Amino Acids, ISSN 0939-4451, E-ISSN 1438-2199, no 36, p. 43-48Article in journal (Refereed)
    Abstract [en]

    Two different assays have been developed and used in order to investigate the optimal conditions for derivatization and detection of acid β-N-methyl-amino-l-alanine (BMAA) in a cyanobacterial sample. BMAA was extracted from cyanobacterial cultures both from the cytosolic (“free”) fraction and in the precipitated (“protein”) fraction using a newly developed extraction scheme and the sample matrix was standardized according to protein concentration to ensure the highest possible derivative yield. A rapid and sensitive HPLC method for fluorescence detection of the non-protein amino acid BMAA in cyanobacteria, utilizing the Waters AccQ-Tag® chemistry and Chromolith® Performance RP-18e columns was developed. Using this new method and utilizing a different buffer system and column than that recommended by Waters, we decreased the time between injections by 75%. The limit of quantification was determined to be 12 nmol and limit of detection as 120 fmol. The linear range was in the range of 8.5 nmol–84 pmol. Accuracy and precision were well within FDA guidelines for bioanalysis.

  • 3.
    Jonasson, Sara
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Berntzon, Lotta
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    A novel cyanobacterial toxin (BMAA) with potential neurodegenerative effects2008In: Plant Biotechnology, ISSN 1342-4580, E-ISSN 1347-6114, Vol. 25, no 3, p. 227-232Article in journal (Refereed)
    Abstract [en]

    The non-protein amino acid beta-N-methyl-amino-L-alanine (BMAA) is a neurotoxin that was recently found to be produced by most cyanobacteria. The neurotoxin was discovered in 1967 in the seeds of the cycad Cycas micronesica, but this BMAA may originate from the symbiotic cyanobacterium Nostoc, which inhabits the roots of cycads. BMAA is thought to be the cause of the deadly neurodegenerative disease amyotrophic lateral sclerosis/parkinsonism dementia complex (ALS/PDC), common among the Chamorro people of Guam. It was demonstrated that the Chamorros, in all probability, have been exposed to high levels of BMAA through dietary consumption of flying foxes which fed mainly on cycads seeds. BMAA production may be a common conserved evolutionary feature among cyanobacteria and due to their wide global distribution, the toxin may be a common concern and potentially involved in provoking degenerative diseases worldwide. BMAA may likewise be bioaccumulated in other cyanobacterial based food webs within ecosystems outside Guam, and it is proposed that such webs may exist in the Baltic Sea, with its massive occurrence of cyanobacteria (blooms).

  • 4.
    Jonasson, Sara
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Berntzon, Lotta
    Stockholm University, Faculty of Science, Department of Botany.
    Spacil, Zdenek
    Stockholm University, Faculty of Science, Department of Analytical Chemistry. Charles University Prague, Czech Republic .
    Ilag, Leopold L.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Ronnevi, Lars-Olof
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure2010In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 107, no 20, p. 9252-9257Article in journal (Refereed)
    Abstract [en]

    beta-methylamino-L-alanine (BMAA), a neurotoxic nonprotein amino acid produced by most cyanobacteria, has been proposed to be the causative agent of devastating neurodegenerative diseases on the island of Guam in the Pacific Ocean. Because cyanobacteria are widespread globally, we hypothesized that BMAA might occur and bioaccumulate in other ecosystems. Here we demonstrate, based on a recently developed extraction and HPLC-MS/MS method and long-term monitoring of BMAA in cyanobacterial populations of a temperate aquatic ecosystem (Baltic Sea, 2007-2008), that BMAA is biosynthesized by cyanobacterial genera dominating the massive surface blooms of this water body. BMAA also was found at higher concentrations in organisms of higher trophic levels that directly or indirectly feed on cyanobacteria, such as zooplankton and various vertebrates (fish) and invertebrates (mussels, oysters). Pelagic and benthic fish species used for human consumption were included. The highest BMAA levels were detected in the muscle and brain of bottom-dwelling fishes. The discovery of regular biosynthesis of the neurotoxin BMAA in a large temperate aquatic ecosystem combined with its possible transfer and bioaccumulation within major food webs, some ending in human consumption, is alarming and requires attention.

  • 5.
    Jonasson, Sara
    et al.
    Stockholm University, Faculty of Science, Department of Botany.
    Vintila, Simina
    Stockholm University, Faculty of Science, Department of Botany.
    Sivonen, Kaarina
    El-Shehawy, Rehab
    Stockholm University, Faculty of Science, Department of Botany.
    Expression of the nodularin synthetase genes in the Baltic Sea bloom-former cyanobacterium Nodularia spumigena strain AV1.2008In: FEMS Microbiol Ecol, ISSN 0168-6496, Vol. 65, no 1, p. 31-39Article in journal (Refereed)
    Abstract [en]

    Cyanobacterial blooms in the Baltic Sea are a common phenomenon and are formed by the heterocystous, filamentous species Nodularia spumigena. The toxicity of these blooms is attributed to the hepatotoxin nodularin, produced by N. spumigena. Little is known regarding the regulatory mechanisms or environmental signaling that control nodularin production. Here we report the characterization of the transcriptional expression pattern of the nodularin synthetase gene cluster (nda) during phosphate depletion, and nitrogen supplementation. Real-time PCR analysis of these genes revealed that while cells continuously expressed the nda cluster, the expression of all nda genes increased when cells were subjected to phosphate depletion, and decreased in the presence of ammonium. In contrast to the shifts in expression, the intracellular and extracellular nodularin concentrations did not vary significantly during the treatments.

  • 6.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Annadotter, Helene
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Biotransfer of beta-N-Methylamino-l-alanine (BMAA) in a Eutrophicated Freshwater Lake2015In: Marine Drugs, ISSN 1660-3397, E-ISSN 1660-3397, Vol. 13, no 3, p. 1185-1201Article in journal (Refereed)
    Abstract [en]

    beta-N-Methylamino-l-alanine (BMAA), a neurotoxic non-protein amino acid, plays a significant role as an environmental risk factor in neurodegenerative diseases, such as amyotrophic lateral sclerosis. BMAA producers occur globally, colonizing almost all habitats and represent species from distinct phytoplanktonic groups, i.e., cyanobacteria, diatoms, and dinoflagellates. Bioaccumulation of BMAA in invertebrate and vertebrate organisms has also been registered around the globe. In the Baltic Sea, BMAA has been detected in several commercial fish species, raising the question of the bioaccumulation of BMAA in Swedish limnic systems. Here we find the presence of BMAA in water samples from Lake Finjasjon and identify its bioaccumulation patterns in both plankti-benthivorous and piscivorous fish, according to fish species, total weight, gender, and season of collection. For the first time, a large number of fish individuals were used in order to draw conclusions on BMAA bioaccumulation in a closed ecological community based on a statistical approach. We may, therefore, conclude that feeding patterns (plankti-benthivorous) and increased age of fish may lead to a higher tissue concentration of BMAA.

  • 7.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Burian, Alfred
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Costa, Pedro Reis
    Annadotter, Heléne
    Godhe, Anna
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    BMAA extraction of cyanobacteria samples: which method to choose?2016In: Environmental science and pollution research international, ISSN 0944-1344, E-ISSN 1614-7499, Vol. 23, no 1, p. 338-350Article in journal (Refereed)
    Abstract [en]

    beta-N-Methylamino-l-alanine (BMAA), a neurotoxin reportedly produced by cyanobacteria, diatoms and dinoflagellates, is proposed to be linked to the development of neurological diseases. BMAA has been found in aquatic and terrestrial ecosystems worldwide, both in its phytoplankton producers and in several invertebrate and vertebrate organisms that bioaccumulate it. LC-MS/MS is the most frequently used analytical technique in BMAA research due to its high selectivity, though consensus is lacking as to the best extraction method to apply. This study accordingly surveys the efficiency of three extraction methods regularly used in BMAA research to extract BMAA from cyanobacteria samples. The results obtained provide insights into possible reasons for the BMAA concentration discrepancies in previous publications. In addition and according to the method validation guidelines for analysing cyanotoxins, the TCA protein precipitation method, followed by AQC derivatization and LC-MS/MS analysis, is now validated for extracting protein-bound (after protein hydrolysis) and free BMAA from cyanobacteria matrix. BMAA biological variability was also tested through the extraction of diatom and cyanobacteria species, revealing a high variance in BMAA levels (0.0080-2.5797 mu g g(-1) DW).

  • 8.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Reis Costa, Pedro
    Moita, Teresa
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Jonasson Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    BMAA in shellfish from two Portuguese transitional water bodies suggests the marine dinoflagellate Gymnodinium catenatum as a potential BMAA source2014In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 152, p. 131-138Article in journal (Refereed)
    Abstract [en]

    The neurotoxin -N-methylamino-l-alanine (BMAA) and its putative role in multiple neurodegenera-tive diseases have been intensely studied since 2005 when the toxin was discovered to be producedby worldwide-distributed cyanobacterial species inhabiting terrestrial, marine, brackish, and freshwaterecosystems. Recently, BMAA production was also associated with one eukaryotic group, namely, diatoms,raising questions about its production by other phytoplanktonic groups. To test for BMAA bioavailabilityin ecosystems where abundant phytoplanktonic blooms regularly occur, samples of filter-feeding shell-fish were collected in two Portuguese transitional water bodies. BMAA content in cockles (Cerastodermaedule) collected weekly between September and November 2009 from Ria de Aveiro and at least once amonth from May to November from Ria Formosa, fluctuated from 0.079 ± 0.055 to 0.354 ± 0.066 g/g DWand from below the limit of detection to 0.434 ± 0.110 g/g DW, respectively. Simultaneously to BMAAoccurrence in cockles, paralytic shellfish toxins were detected in shellfish as a result of Gymnodiniumcatenatum blooms indicating a possible link between this marine dinoflagellate and BMAA production.Moreover, considerable high BMAA levels, 0.457 ± 0.186 g/g DW, were then determined in a laboratorygrown culture of G. catenatum. This work reveals for the first time the presence of BMAA in shellfishfrom Atlantic transitional water bodies and consubstantiate evidences of G. catenatum as one of the mainsources of BMAA in these ecosystems.

  • 9.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ström, Linnea
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Godhe, Anna
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kinetics of beta-N-methylamino-L-alanine (BMAA) and 2, 4-diaminobutyric acid (DAB) production by diatoms: the effect of nitrogen2019In: European journal of phycology, ISSN 0967-0262, E-ISSN 1469-4433, Vol. 54, no 1, p. 115-125Article in journal (Refereed)
    Abstract [en]

    The neurotoxins beta-N-methylamino-L-alanine (BMAA) and 2,4-diaminobutyric acid (DAB) are produced by cyanobacteria, diatoms and dinoflagellates and have been detected in seafood worldwide. Our present knowledge of their metabolism or biosynthesis is limited. In this study, the production of BMAA and DAB as a function of time was monitored in five strains representing four species of diatoms, i.e. Phaeodactylum tricornutum, Thalassiosira weissflogii, Thalassiosira pseudonana and Navicula pelliculosa, previously identified as BMAA and DAB producers. Subsequently, three strains were selected and exposed to three nitrogen treatments - starvation, control (the standard concentration in f/2 medium) and enrichment, because BMAA metabolism has been suggested to be closely associated with cellular nitrogen metabolism in both cyanobacteria and diatoms. Chlorophyll a and total protein concentrations were also determined. Our results indicate that BMAA and DAB production in diatoms is species- and strain-specific. However, production might also be affected by stress, particularly as related to nitrogen starvation and cell density. Furthermore, this study shows a significant correlation between the production of the two neurotoxins which might further suggest common steps in the metabolic pathways.

  • 10.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ström, Linnea
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Godhe, Anna
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    The effect of exogenous beta-N-methylamino-L-alanine (BMAA) on the diatoms Phaeodactylum tricornutum and Thalassiosira weissflogii2016In: Harmful Algae, ISSN 1568-9883, E-ISSN 1878-1470, Vol. 58, p. 85-92Article in journal (Refereed)
    Abstract [en]

    beta-N-methylamino-L-alanine (BMAA), a non-protein amino acid with neurodegenerative features, is known to be produced by cyanobacteria, diatoms and a dinoflagellate. BMAA research has intensified over the last decade, and knowledge has been gained about its bioaccumulation in aquatic and terrestrial ecosystems, toxic effects in model organisms and neurotoxicity in vivo and in vitro. Nevertheless, knowledge of the actual physiological role of BMAA in the producing species or of the ecological factors that regulate BMAA production is still lacking. A few studies propose that BMAA functions to signal nitrogen depletion in cyanobacteria. To investigate whether BMAA might have a similar role in diatoms, two diatom species - Phaeodactylum tricornutum and Thalassiosira weissflogii - were exposed to exogenous BMAA at environmental relevant concentrations, i.e. 0.005, 0.05 and 0.5 mu M. BMAA was taken up in a concentration dependent manner in both species in the BMAA free fraction and in the protein fraction of T. weissflogii. As a result of the treatments, the diatom cells at some of the time points and at some of the BMAA concentrations exhibited lower concentrations of chlorophyll a and protein, in comparison to controls. At the highest (0.5 mu M) concentration of BMAA, extracellular ammonia was found in the media of both species at all time points. These results suggest that BMAA interferes with nitrogen metabolism in diatoms, possibly by inhibiting ammonium assimilation via the GS/GOGAT pathway.

  • 11.
    Lage, Sandra
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Ström, Linnea
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Godhe, Anna
    Rydberg, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    The effect of exogenous β-N-methylamino-L-alanine on the diatoms Phaeodactylum tricornutum and Thalassiosira weissflogii Manuscript (preprint) (Other academic)
  • 12.
    Spacil, Zdenek
    et al.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Eriksson, Johan
    Stockholm University, Faculty of Science, Department of Botany.
    Jonasson, Sara
    Stockholm University, Faculty of Science, Department of Botany.
    Rasmussen, Ulla
    Stockholm University, Faculty of Science, Department of Botany.
    Ilag, Leopold L.
    Stockholm University, Faculty of Science, Department of Analytical Chemistry.
    Bergman, Birgitta
    Stockholm University, Faculty of Science, Department of Botany.
    Analytical protocol for identification of BMAA and DAB in biologicalsamples2010In: The Analyst, ISSN 0003-2654, E-ISSN 1364-5528, Vol. 135, p. 127-132Article in journal (Refereed)
    Abstract [en]

     

    b

    -N-methylamino-L-alanine (BMAA) is a non-protein amino acid, thought to be inflicting neurodegenerative diseases related to ALS/PDC in human beings. Due to conflicting data concerning the presence of BMAA in various biological matrixes, we present a robust and sensitive method for high confidence identification of BMAA after derivatization by 6-aminoquinolyl-N

    -hydroxysuccinimidyl carbamate (AQC). The efficient sample pretreatment in combination with LC-MS/MS SRM enables chromatographic separation of BMAA from the isomer 2,3-diaminobutyric acid (DAB). The method is applicable for selective BMAA/DAB detection in various biological samples ranging from a prokaryotic cyanobacterium to eukaryotic fish.

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