Frontiers in Microbiology (Feb 2021)

Temporal Patterns and Intra- and Inter-Cellular Variability in Carbon and Nitrogen Assimilation by the Unicellular Cyanobacterium Cyanothece sp. ATCC 51142

  • Lubos Polerecky,
  • Takako Masuda,
  • Meri Eichner,
  • Meri Eichner,
  • Sophie Rabouille,
  • Sophie Rabouille,
  • Marie Vancová,
  • Michiel V. M. Kienhuis,
  • Gabor Bernát,
  • Gabor Bernát,
  • Jose Bonomi-Barufi,
  • Douglas Andrew Campbell,
  • Pascal Claquin,
  • Jan Červený,
  • Mario Giordano,
  • Mario Giordano,
  • Eva Kotabová,
  • Jacco Kromkamp,
  • Ana Teresa Lombardi,
  • Martin Lukeš,
  • Ondrej Prášil,
  • Susanne Stephan,
  • Susanne Stephan,
  • David Suggett,
  • Tomas Zavřel,
  • Kimberly H. Halsey

DOI
https://doi.org/10.3389/fmicb.2021.620915
Journal volume & issue
Vol. 12

Abstract

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Unicellular nitrogen fixing cyanobacteria (UCYN) are abundant members of phytoplankton communities in a wide range of marine environments, including those with rapidly changing nitrogen (N) concentrations. We hypothesized that differences in N availability (N2 vs. combined N) would cause UCYN to shift strategies of intracellular N and C allocation. We used transmission electron microscopy and nanoscale secondary ion mass spectrometry imaging to track assimilation and intracellular allocation of 13C-labeled CO2 and 15N-labeled N2 or NO3 at different periods across a diel cycle in Cyanothece sp. ATCC 51142. We present new ideas on interpreting these imaging data, including the influences of pre-incubation cellular C and N contents and turnover rates of inclusion bodies. Within cultures growing diazotrophically, distinct subpopulations were detected that fixed N2 at night or in the morning. Additional significant within-population heterogeneity was likely caused by differences in the relative amounts of N assimilated into cyanophycin from sources external and internal to the cells. Whether growing on N2 or NO3, cells prioritized cyanophycin synthesis when N assimilation rates were highest. N assimilation in cells growing on NO3 switched from cyanophycin synthesis to protein synthesis, suggesting that once a cyanophycin quota is met, it is bypassed in favor of protein synthesis. Growth on NO3 also revealed that at night, there is a very low level of CO2 assimilation into polysaccharides simultaneous with their catabolism for protein synthesis. This study revealed multiple, detailed mechanisms underlying C and N management in Cyanothece that facilitate its success in dynamic aquatic environments.

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