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

Polerecky, L; Masuda, T; Eichner, M; Rabouille, S; Vancová, M; Kienhuis, MVM; Bernát, G; Bonomi-Barufi, J; Campbell, DA; Claquin, P; Červený, J; Giordano, M; Kotabová, E; Kromkamp, J; Lombardi, AT; Lukeš, M; Prášil, O; Stephan, S; Suggett, D; Zavřel, T; Halsey, KH

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

Polerecky, L Masuda, T Eichner, M Rabouille, S Vancová, M Kienhuis, MVM Bernát, G Bonomi-Barufi, J Campbell, DA Claquin, P Červený, J Giordano, M Kotabová, E Kromkamp, J Lombardi, AT Lukeš, M Prášil, O Stephan, S Suggett, D

Zavřel, T Halsey, KH

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Publisher:: Frontiers Media SA
Publication Type:: Journal Article
Citation:: Frontiers in Microbiology, 2021, 12, pp. 620915
Issue Date:: 2021-02-04

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Field	Value	Language
dc.contributor.author	Polerecky, L
dc.contributor.author	Masuda, T
dc.contributor.author	Eichner, M
dc.contributor.author	Rabouille, S
dc.contributor.author	Vancová, M
dc.contributor.author	Kienhuis, MVM
dc.contributor.author	Bernát, G
dc.contributor.author	Bonomi-Barufi, J
dc.contributor.author	Campbell, DA
dc.contributor.author	Claquin, P
dc.contributor.author	Červený, J
dc.contributor.author	Giordano, M
dc.contributor.author	Kotabová, E
dc.contributor.author	Kromkamp, J
dc.contributor.author	Lombardi, AT
dc.contributor.author	Lukeš, M
dc.contributor.author	Prášil, O
dc.contributor.author	Stephan, S
dc.contributor.author	Suggett, D https://orcid.org/0000-0001-5326-2520
dc.contributor.author	Zavřel, T
dc.contributor.author	Halsey, KH
dc.date.accessioned	2021-03-01T21:47:20Z
dc.date.available	2021-03-01T21:47:20Z
dc.date.issued	2021-02-04
dc.identifier.citation	Frontiers in Microbiology, 2021, 12, pp. 620915
dc.identifier.issn	1664-302X
dc.identifier.issn	1664-302X
dc.identifier.uri	http://hdl.handle.net/10453/146597
dc.description.abstract	<jats:p>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 (N<jats:sub>2</jats:sub> 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 <jats:sup>13</jats:sup>C-labeled CO<jats:sub>2</jats:sub> and <jats:sup>15</jats:sup>N-labeled N<jats:sub>2</jats:sub> or NO<jats:sub>3</jats:sub> at different periods across a diel cycle in <jats:italic>Cyanothece</jats:italic> 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 N<jats:sub>2</jats:sub> 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 N<jats:sub>2</jats:sub> or NO<jats:sub>3</jats:sub>, cells prioritized cyanophycin synthesis when N assimilation rates were highest. N assimilation in cells growing on NO<jats:sub>3</jats:sub> 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 NO<jats:sub>3</jats:sub> also revealed that at night, there is a very low level of CO<jats:sub>2</jats:sub> assimilation into polysaccharides simultaneous with their catabolism for protein synthesis. This study revealed multiple, detailed mechanisms underlying C and N management in <jats:italic>Cyanothece</jats:italic> that facilitate its success in dynamic aquatic environments.</jats:p>
dc.language	en
dc.publisher	Frontiers Media SA
dc.relation.ispartof	Frontiers in Microbiology
dc.relation.isbasedon	10.3389/fmicb.2021.620915
dc.rights	info:eu-repo/semantics/openAccess
dc.subject	0502 Environmental Science and Management, 0503 Soil Sciences, 0605 Microbiology
dc.title	Temporal Patterns and Intra- and Inter-Cellular Variability in Carbon and Nitrogen Assimilation by the Unicellular Cyanobacterium Cyanothece sp. ATCC 51142
dc.type	Journal Article
utslib.citation.volume	12
utslib.for	0502 Environmental Science and Management
utslib.for	0503 Soil Sciences
utslib.for	0605 Microbiology
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - C3 - Climate Change Cluster
pubs.organisational-group	/University of Technology Sydney
utslib.copyright.status	open_access	*
dc.date.updated	2021-03-01T21:47:18Z
pubs.publication-status	Published online
pubs.volume	12

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 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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http://hdl.handle.net/10453/146597