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Early-earth nonprotein amino acid metabolites in modern cyanobacterial microbialites

  • Stephanie L. Bishop
  • Fiona J. M. Tymm
  • Karen Perry
  • Jeff K. Kerkovius
  • Frederic Menard
  • Allyson Brady
  • Greg Slater
  • Darlene S. S. Lim
  • James S. Metcalf
  • Sandra A. Banack
  • Paul A. Cox
  • Susan J. MurchEmail author
Original Paper
  • 29 Downloads

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.

Keywords

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

Notes

Acknowledgements

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

Author contributions

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.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

10311_2019_943_MOESM1_ESM.docx (7.4 mb)
Supplementary material 1 (DOCX 7561 kb)

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Stephanie L. Bishop
    • 1
  • Fiona J. M. Tymm
    • 1
  • Karen Perry
    • 1
  • Jeff K. Kerkovius
    • 1
  • Frederic Menard
    • 1
  • Allyson Brady
    • 2
  • Greg Slater
    • 2
  • Darlene S. S. Lim
    • 3
  • James S. Metcalf
    • 4
  • Sandra A. Banack
    • 4
  • Paul A. Cox
    • 4
  • Susan J. Murch
    • 1
    Email author
  1. 1.Chemistry, Room 350 Fipke CentreUniversity of British ColumbiaKelownaCanada
  2. 2.School of Geography and Earth SciencesMcMaster UniversityHamiltonCanada
  3. 3.NASA Ames Research CenterMoffett FieldUSA
  4. 4.Brain Chemistry LabsInstitute for EthnomedicineJackson HoleUSA

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