Temporal Patterns and Intra- and Inter-Cellular Variability in Carbon and Nitrogen Assimilation by the Unicellular Cyanobacterium Cyanothece sp. ATCC 51142
Polerecky, Lubos; Masuda, Takako; Eichner, Meri; Rabouille, Sophie; Vancová, Marie; Kienhuis, Michiel V.M.; Bernát, Gabor; Bonomi-Barufi, Jose; Campbell, Douglas Andrew; Claquin, Pascal; Červený, Jan; Giordano, Mario; Kotabová, Eva; Kromkamp, Jacco; Lombardi, Ana Teresa; Lukeš, Martin; Prášil, Ondrej; Stephan, Susanne; Suggett, David; Zavřel, Tomas; Halsey, Kimberly H.
(2021) Frontiers in Microbiology, volume 12, pp.
(Article)
Abstract
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
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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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Keywords: carbon fixation, Crocosphaera subtropica (former Cyanothece sp. ATCC 51142), Cyanothece, nanoSIMS, nitrogen fixation, photosynthesis, TEM, Microbiology, Microbiology (medical)
ISSN: 1664-302X
Publisher: Frontiers Media S.A.
Note: Funding Information: This work results from the 10th Group for Aquatic Photosynthesis (GAP) workshop held in T?ebo?, Czech Republic, in August 2017 and subsequent discussions. With this contribution, we wish to honor the late MG and JK for their collegiality, friendship, and extensive contributions to the field of phytoplankton ecophysiology. Funding. The NanoSIMS facility at Utrecht University was financed through a large infrastructure grant by the Netherlands Organization for Scientific Research (NWO; grant no. 175.010.2009.011). Electron microscopy was supported by the Czech Ministry of Education, Youth and Sport through the BioImaging Research Infrastructure project LM2015062. GB was supported by the Hungarian Academic Foundation (OTKA, grant no. K128950). TZ and J? were supported by the Ministry of Education, Youth and Sports of the Czech Republic (OP RDE grant number CZ.02.1.01/0.0/0.0/16?026/0008413) and by the Czech Science Foundation (GA CR, grant number 18?24397S). SR acknowledges support from the LEFE-INSU funding program. TM, OP, and ME were supported by the Czech Science Foundation (GACR 20-17627S and 20-02827Y). SS was supported by the ILES (Illuminating Lake Ecosystem) project funded through the Leibniz Competition (SAW-2015-IGB-1). Publisher Copyright: © Copyright © 2021 Polerecky, Masuda, Eichner, Rabouille, Vancová, Kienhuis, Bernát, Bonomi-Barufi, Campbell, Claquin, Červený, Giordano, Kotabová, Kromkamp, Lombardi, Lukeš, Prášil, Stephan, Suggett, Zavřel and Halsey.
(Peer reviewed)