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Proteomic changes orchestrate metabolic acclimation of a unicellular diazotrophic cyanobacterium during light-dark cycle and nitrogen fixation states

ABSTRACT: Cyanobacteria have developed an impressive array of proteins and pathways, each tailored for specific metabolic attributes, to execute photosynthesis and biological nitrogen (N2)-fixation. An understanding of these biologically incompatible processes provides important insights into how they can be optimized for renewable energy. To expand upon our current knowledge, we performed label-free quantitative proteomic analysis of the unicellular diazotrophic cyanobacterium Crocosphaera subtropica ATCC 51142 grown with and without nitrate under 12-hour light-dark cycles. Results showed significant shift in metabolic activities including photosynthesis, respiration, biological nitrogen fixation (BNF), and proteostasis to different growth conditions. We identified more than 20 nitrogenase enzymes which were among the most highly expressed proteins in the dark under nitrogen-fixing conditions, emphasizing their importance in BNF. Nitrogenase enzymes were not expressed under non nitrogen fixing conditions, suggesting a regulatory mechanism based on nitrogen availability. The synthesis of key respiratory enzymes and uptake hydrogenase (HupSL) synchronized with the synthesis of nitrogenase indicating a coordinated regulation of processes involved in energy production and BNF. Data suggests alternative pathways that cells utilize, such as oxidative pentose phosphate (OPP) and 2-oxoglutarate (2-OG) pathways, to produce ATP and support bioenergetic BNF. Data also indicates the important role of uptake hydrogenase for the removal of O2 to support BNF. Overall, this study expands upon our knowledge regarding molecular responses of Crocosphaera 51142 to nitrogen and light-dark phases, shedding light on potential applications and optimization for renewable energy.

INSTRUMENT(S): Orbitrap Fusion Lumos

ORGANISM(S): Crocosphaera Subtropica (ncbitaxon:2546360)

SUBMITTER: Uma Aryal

PROVIDER: MSV000094471 | MassIVE | Thu Apr 04 14:43:00 BST 2024

REPOSITORIES: MassIVE

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Project description:Transcriptional response of the photoheterotrophic marine bacterium D. shibea to changing light regimes. Second part of the study analysing the transition from photoheterotrophic light to heterotrophic dark growth. Bacterial aerobic anoxygenic photosynthesis (AAP) is an important mechanism of energy gain in aquatic habitats, accounting for up to 5% of the surface ocean’s photosynthetic electron transport. The dominant AAP bacteria in marine communities belong to the Roseobacter clade. For this reason we used Dinoroseobacter shibae as a model organism to study the transcriptional response of AAP bacteria to changing light regimes. We used continuous cultivation of D. shibae in a chemostat in combination with time series microarray analysis in order to identify gene regulatory patterns after a change in illumination. The change from heterotrophic growth in the dark to photoheterotrophic growth in the light was accompanied by a strong but transient activation of a broad stress response to cope with the formation of harmful singlet oxygen during photophosphorylation, an immediate downregulation of photosynthesis-related genes, fine-tuning of the expression of electron transport chain components and upregulation of the transcriptional and translational apparatus. Furthermore, our data indicate that D. shibae might use the 3-hydroxypropionate cycle for CO2 fixation. Analysis of the transcriptome dynamics after the switch from light to dark demonstrates that only few genes are directly regulated in response to light and other signals such as singlet oxygen concentration, electron flow, redox status and energy charge of the cell must be involved in the regulation of the processes accompanying AAP. Based on the transcriptome data first hypothesis about transcriptional control of AAP could be formulated. This study provides the first analysis of AAP on the level of transcriptome dynamics. Our data allow the formulation of testable hypotheses about the mechanisms involved in the regulation of this important biological process. Samples from light grown cells were used as a reference, 6 timepoints in the dark, biological replicates: 2

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Proteomic changes orchestrate metabolic acclimation of a unicellular diazotrophic cyanobacterium during light-dark cycle and nitrogen fixation states

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