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Abstract
ABSTRACTUnder diazotrophic conditions, the model filamentous, heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 develops a metabolic strategy based on the physical separation of the processes of oxygenic photosynthesis, in vegetative cells, and N2 fixation, in heterocysts. This strategy requires the exchange of carbon and nitrogen metabolites and their distribution along the filaments, which takes place through molecular diffusion via septal junctions involving FraCD proteins. Here, Anabaena was incubated in a time course (up to 20 h) with [13C]bicarbonate and 15N2 and analyzed by secondary ion mass spectrometry imaging (SIMS) (large-geometry SIMS [LG-SIMS] and NanoSIMS) to quantify C and N assimilation and distribution in the filaments. The 13C/12C and 15N/14N ratios measured in wild-type filaments showed a general increase with time. The enrichment was relatively homogeneous in vegetative cells along individual filaments, while it was reduced in heterocysts. Heterocysts, however, accumulated recently fixed N at their poles, in which the cyanophycin plug [multi-l-arginyl-poly(l-aspartic acid)] is located. In contrast to the rather homogeneous label found along stretches of vegetative cells, 13C/12C and 15N/14N ratios were significantly different between filaments both at the same and different time points, showing high variability in metabolic states. A fraC fraD mutant did not fix N2, and the 13C/12C ratio was homogeneous along the filament, including the heterocyst in contrast to the wild type. Our results show the consumption of reduced C in the heterocysts associated with the fixation and export of fixed N and present an unpredicted heterogeneity of cellular metabolic activity in different filaments of an Anabaena culture under controlled conditions.
Highlights
Under diazotrophic conditions, the model filamentous, heterocystforming cyanobacterium Anabaena sp. strain PCC 7120 develops a metabolic strategy based on the physical separation of the processes of oxygenic photosynthesis, in vegetative cells, and N2 fixation, in heterocysts
Nieves-Morión et al Heterocyst-forming cyanobacteria of the order Nostocales grow as long chains of cells, in which the absence of combined nitrogen triggers a cell differentiation process resulting in two cell types along filaments: vegetative cells and heterocysts [1]
The intercellular molecular exchange in filamentous cyanobacteria has been studied in real time by fluorescence recovery after photobleaching (FRAP) analysis using fluorescent markers [8], which has indicated that exchange takes place by means of molecular diffusion through cell-cell joining structures termed septal junctions (9; reviewed in references 10 and 11)
Summary
The model filamentous, heterocystforming cyanobacterium Anabaena sp. strain PCC 7120 develops a metabolic strategy based on the physical separation of the processes of oxygenic photosynthesis, in vegetative cells, and N2 fixation, in heterocysts. Strain PCC 7120 develops a metabolic strategy based on the physical separation of the processes of oxygenic photosynthesis, in vegetative cells, and N2 fixation, in heterocysts This strategy requires the exchange of carbon and nitrogen metabolites and their distribution along the filaments, which takes place through molecular diffusion via septal junctions involving FraCD proteins. Heterocyst differentiation involves a specific program of gene expression producing filaments that contain intercalary heterocysts that, in most cases, are spaced by 10 to 15 vegetative cells along the filament [1] This process is a way to separate oxygenic photosynthesis and N2 fixation, which are incompatible metabolic activities because nitrogenase is inactivated in the presence of oxygen [7]. A study comparing C and N enrichment and distribution between different filaments in a culture is not available
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