Skip to main content
SpringerLink
Log in

The Effect of Exogenous β-N-Methylamino-l-alanine on the Growth of Synechocystis PCC6803

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

β-N-Methylamino-l-alanine (BMAA), a non-proteinogenic amino acid, has been detected in a range of cyanobacteria, including terrestrial, aquatic, free living and endosymbiotic species. The widespread occurrence of cyanobacteria in the environment raises concerns regarding the ecological and toxicological impact of BMAA, and consequently, studies have focussed extensively on the toxicity and environmental impact of BMAA, while no research has addressed the ecophysiological or metabolic role of the compound in cyanobacteria. In this study, both the uptake of exogenous BMAA by and the effect of exogenous BMAA on the growth of Synechocystis PCC6803 were investigated. BMAA was rapidly taken up by the non-diazotrophic cyanobacterium Synechocystis PCC6803 in a concentration dependent manner. The presence of exogenous BMAA resulted in a substantial and concentration-dependent decrease in cell growth and the substantial loss of photosynthetic pigmentation. Similar effects were seen in the presence of the non-proteinogenic amino acid, 2,4-diaminobutyric acid but to a lesser degree than that of BMAA. The effects were reversed when light was decreased from 16 to 10 μmol m−2 s−1. Control cultures grown in the presence of l-arginine, l-asparagine, l-glutamate and glycine showed normal or slightly increased growth with no change in pigmentation. The decrease in growth rate coupled to bleaching indicates that BMAA may induce chlorosis in the presence of adequate photosynthetic radiation suggesting a connection between BMAA and the induction of conditions, such as nitrogen or sulphur depletion, that result in growth arrest and the induction of chlorosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Anderson SL, McIntosh L (1991) Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. PCC6803: a blue-light-requiring process. J Bacteriol 173(9):2761–2767

    PubMed  CAS  Google Scholar 

  2. Banack SA, Johnson HE, Cheng R, Cox PA (2007) Production of neurotoxic BMAA by marine cyanobacteria. Mar Drugs 5:180–196

    Article  PubMed  CAS  Google Scholar 

  3. Banack SA, Downing TG, Spacil Z, Purdie EL, Metcalf JS, Downing S, Esterhuizen M, Codd GA, Cox PA (2010) Distinguishing the cyanobacterial neurotoxin β-N-methylamino-L-alanine (BMAA) from its structural isomer 2,4-diaminobutyric acid (2,4-DAB). Toxicon 56(6):868–879

    Article  PubMed  CAS  Google Scholar 

  4. Brenner ED, Martinez-Barboza N, Clark AP, Liang QS, Stevenson DW, Coruzzi GM (2000) Arabidopsis mutants resistant to S(+)-b-methyl-a, b-diaminopropionic acid, a cycad-derived glutamate receptor agonist. Plant Physiol 124:1615–1624

    Article  PubMed  CAS  Google Scholar 

  5. Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci USA 100:13380–13383

    Article  PubMed  CAS  Google Scholar 

  6. Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce β-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102:5074–5078

    Article  PubMed  CAS  Google Scholar 

  7. Esterhuizen M, Downing TG (2008) β-N-Methylamino-L-alanine (BMAA) in novel South African cyanobacterial isolates. Ecotoxicol Environ Saf 71:309–313

    Article  PubMed  CAS  Google Scholar 

  8. Esterhuizen M, Pflugmacher S, Downing TG (2011) β-N-Methylamino-L-alanine (BMAA) uptake by the aquatic macrophyte Ceratophyllum demersum. Ecotoxicol Environ Saf 74(1):74–77

    Article  PubMed  CAS  Google Scholar 

  9. Esterhuizen M, Downing S, Downing TG (2011) Improved sensitivity using liquid chromatography mass spectrometry (LC-MS) for detection of propyl chloroformate derivatised β-N-methylamino-L-alanine (BMAA) in cyanobacteria. Water SA 37(2):133–138

    Google Scholar 

  10. Flores E, Herrero A (1994) Assimilatory nitrogen metabolism and its regulation. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic, Dordrecht, pp 487–517

    Google Scholar 

  11. Kurland LT (1972) An appraisal of the neurotoxicity of cycad and the etiology of amyotrophic lateral sclerosis on Guam. Fed Proc 31:1540–1542

    PubMed  CAS  Google Scholar 

  12. Montesinos ML, Herrero A, Flores E (1995) Amino acid transport systems required for diazotrophic growth in the cyanobacterium Anabaena sp. strain PCC7120. J Bacteriol 177(11):3150–3157

    PubMed  CAS  Google Scholar 

  13. Rippka R (1988) Isolation and purification of cyanobacteria. Methods Enzymol 167:3–27

    Article  PubMed  CAS  Google Scholar 

  14. Ping X, McAuley PJ (1990) Uptake of amino acids by the cyanobacterium Anabaena ATCC 27893. New Phytol 115:581–585

    Article  Google Scholar 

  15. Sauer J, Schreiber U, Schmid R, Völker U, Forchhammer K (2001) Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. Plant Physiol 126:233–243

    Article  PubMed  CAS  Google Scholar 

  16. Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiol 151:2503–2514

    Article  CAS  Google Scholar 

  17. Spencer PS, Nunn PB, Hugon J, Ludolph AC, Ross SM, Roy DN, Robertson RC (1987) Guam amyotrophic lateral sclerosis–parkinsonism–dementia linked to a plant excitant neurotoxin. Science 237(4814):517–522

    Article  PubMed  CAS  Google Scholar 

  18. Weathers PJ, Chee HL, Allen MM (1978) Arginine catabolism in Aphanocapsa 6308. Arch Microbiol 118:1–6

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by the Water Research Commission of South Africa project K5/1885.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Microbiology, Nelson Mandela Metropolitan University, PO Box 77000, Port Elizabeth, 6031, South Africa

    Simoné Downing, Maryna van de Venter & Timothy G. Downing

Authors
  1. Simoné Downing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maryna van de Venter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy G. Downing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy G. Downing.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Downing, S., van de Venter, M. & Downing, T.G. The Effect of Exogenous β-N-Methylamino-l-alanine on the Growth of Synechocystis PCC6803. Microb Ecol 63, 149–156 (2012). https://doi.org/10.1007/s00248-011-9958-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-011-9958-9

Keywords

Search

Navigation