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Early-earth nonprotein amino acid metabolites in modern cyanobacterial microbialites

Abstract

Cyanobacteria are among the earth’s oldest known living groups of organisms and can form layered accretions called microbialites, found in both the fossil record and existing lakes. Studies of cyanobacterial biochemical processes help to understand the evolution of life on earth. The conserved metabolism of cyanobacterial species includes the biosynthesis of unusual nonprotein amino acids such as N-(2-aminoethyl)glycine, hypothesized to have constituted an early form of genetic information in cells. Pavilion Lake in British Columbia, Canada, hosts a population of unique, actively growing microbialites covered in biofilms dominated by cyanobacteria. We hypothesized that the living microbial communities produce dinitrogenous nonprotein amino acids, such as N-(2-aminoethyl)glycine and its structural isomers β-N-methylamino-l-alanine, 2,4-diaminobutyric acid and β-aminomethyl-l-alanine. We analyzed samples in sediment traps collected between 2007 and 2014 in depths ranging from 11 to 46 m. N-(2-aminoethyl)glycine, 2,4-diaminobutyric acid and β-aminomethyl-l-alanine were found in highest concentration in the shallowest microbialite biofilms with a maximum of 22 ng/g, 33 ng/g and 0.4 ng/g, respectively. In contrast, the concentration of β-N-methylamino-l-alanine was highest in collections between 18 and 26 m depths and only β-N-methylamino-l-alanine was found in the deepest water collections. These data provide evidence indicating that the production of these nonprotein amino acids is highly conserved through the evolution of cyanobacteria and suggest that the nitrogen-rich metabolites may have had both an important role in ancient and modern cyanobacterial metabolism. Further research will determine the role of N-(2-aminoethyl)glycine and its isomers in early life metabolism and their current function in photosynthetic cells.

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Acknowledgements

Funding support from the Natural Sciences and Engineering Council of Canada (NSERC) is gratefully acknowledged.

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SJM, KP and PAC conceived and designed the research study. JKK and FM developed a custom synthesis method for β-aminomethyl-l-alanine and synthesized the analytical standard for method optimization. AB, GS and DSSL performed studies to characterize the microbialites in Pavilion Lake, collected, curated and shared the samples analyzed in this study. FJMT, SLB, JSM and SAB developed analytical methods and conducted the experiments. FJMT, SLB and SJM performed the statistical analysis and data interpretation. All authors read and approved the final manuscript.

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Correspondence to Susan J. Murch.

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The authors declare no competing interests.

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Bishop, S.L., Tymm, F.J.M., Perry, K. et al. Early-earth nonprotein amino acid metabolites in modern cyanobacterial microbialites. Environ Chem Lett 18, 467–473 (2020). https://doi.org/10.1007/s10311-019-00943-4

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  • DOI: https://doi.org/10.1007/s10311-019-00943-4

Keywords

  • Pavilion Lake
  • N-(2-aminoethyl)glycine (AEG)
  • β-N-methylamino-l-alanine (BMAA)
  • Microbialites
  • Cyanobacteria
  • Microbial biofilms