Culturing synechocystis sp. Strain pcc 6803 with N2 and CO2 in a diel regime reveals multiphase glycogen dynamics with low maintenance costs

A. Angermayr, P. Van Alphen, D. Hasdemir, G. Kramer, M. Iqbal, W. Van Grondelle, H. Hoefsloot, Y. Choi, K. Hellingwerf, Applied and Environmental Microbiology 82 (2016) 4180–4189.


Journal Article | Published | English
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Abstract
Investigating the physiology of cyanobacteria cultured under a diel light regime is relevant for a better understanding of the resulting growth characteristics and for specific biotechnological applications that are foreseen for these photosynthetic organisms. Here, we present the results of a multiomics study of the model cyanobacterium Synechocystis sp. strain PCC 6803, cultured in a lab-scale photobioreactor in physiological conditions relevant for large-scale culturing. The culture was sparged withN2 andCO2, leading to an anoxic environment during the dark period. Growth followed the availability of light. Metabolite analysis performed with 1Hnuclear magnetic resonance analysis showed that amino acids involved in nitrogen and sulfur assimilation showed elevated levels in the light. Most protein levels, analyzed through mass spectrometry, remained rather stable. However, several high-light-response proteins and stress-response proteins showed distinct changes at the onset of the light period. Microarray-based transcript analysis found common patterns of~56% of the transcriptome following the diel regime. These oscillating transcripts could be grouped coarsely into genes that were upregulated and downregulated in the dark period. The accumulated glycogen was degraded in the anaerobic environment in the dark. A small part was degraded gradually, reflecting basic maintenance requirements of the cells in darkness. Surprisingly, the largest part was degraded rapidly in a short time span at the end of the dark period. This degradation could allow rapid formation of metabolic intermediates at the end of the dark period, preparing the cells for the resumption of growth at the start of the light period.
Publishing Year
Date Published
2016-07-01
Journal Title
Applied and Environmental Microbiology
Acknowledgement
Dutch Ministry of Economic Affairs, Agriculture, and Innovation through the program BioSolar CellsS. Andreas Angermayr,Pascal van Alphen, Klaas J. Hellingwerf We thank Naira Quintana (presently at Rousselot, Belgium) for the ini- tiative at the 10th Cyanobacterial Molecular Biology Workshop (CMBW), June 2010, Lake Arrowhead, Los Angeles, CA, USA, to start the collaborative endeavor reported here. We thank Timo Maarleveld from CWI/VU (Amsterdam) for a custom-made Python script handling the output from the NMR analysis and for evaluating and visualizing the separate metabolites for their evaluation. We thank Rob Verpoorte from Leiden University (metabolome analysis) and Hans Aerts from the AMC (proteome analysis) for lab space and equipment. We thank Robert Leh- mann (Humboldt University Berlin) and Ilka Axmann (University of Düsseldorf) for sharing the R-code for the LOS transformation of the transcript data. We thank Hans C. P. Matthijs from IBED for inspiring dialogues and insightful thoughts on continuous culturing of cyanobac- teria. We thank Sandra Waaijenborg for performing the transcript nor- malization and Johan Westerhuis from BDA, Jeroen van der Steen and Filipe Branco dos Santos from MMP, and Lucas Stal from IBED/NIOZ for helpful discussions. We thank Milou Schuurmans from MMP for help with sampling and glycogen determination. We thank the members of the RNA Biology & Applied Bioinformatics group at SILS, in particular Selina van Leeuwen, Elisa Hoekstra, and Martijs Jonker, for the microarray anal- ysis. We thank the reviewers of this work for their insightful comments which improved the quality of the manuscript. This work, including the efforts of S. Andreas Angermayr, Pascal van Alphen, and Klaas J. Hellingwerf, was funded by Dutch Ministry of Eco- nomic Affairs, Agriculture, and Innovation through the program BioSolar Cells.
Volume
82
Issue
14
Page
4180 - 4189
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Cite this

Angermayr A, Van Alphen P, Hasdemir D, et al. Culturing synechocystis sp. Strain pcc 6803 with N2 and CO2 in a diel regime reveals multiphase glycogen dynamics with low maintenance costs. Applied and Environmental Microbiology. 2016;82(14):4180-4189. doi:10.1128/AEM.00256-16
Angermayr, A., Van Alphen, P., Hasdemir, D., Kramer, G., Iqbal, M., Van Grondelle, W., … Hellingwerf, K. (2016). Culturing synechocystis sp. Strain pcc 6803 with N2 and CO2 in a diel regime reveals multiphase glycogen dynamics with low maintenance costs. Applied and Environmental Microbiology, 82(14), 4180–4189. https://doi.org/10.1128/AEM.00256-16
Angermayr, Andreas, Pascal Van Alphen, Dicle Hasdemir, Gertjan Kramer, Muzamal Iqbal, Wilmar Van Grondelle, Huub Hoefsloot, Younghae Choi, and Klaas Hellingwerf. “Culturing Synechocystis Sp. Strain Pcc 6803 with N2 and CO2 in a Diel Regime Reveals Multiphase Glycogen Dynamics with Low Maintenance Costs.” Applied and Environmental Microbiology 82, no. 14 (2016): 4180–89. https://doi.org/10.1128/AEM.00256-16.
A. Angermayr et al., “Culturing synechocystis sp. Strain pcc 6803 with N2 and CO2 in a diel regime reveals multiphase glycogen dynamics with low maintenance costs,” Applied and Environmental Microbiology, vol. 82, no. 14, pp. 4180–4189, 2016.
Angermayr A, Van Alphen P, Hasdemir D, Kramer G, Iqbal M, Van Grondelle W, Hoefsloot H, Choi Y, Hellingwerf K. 2016. Culturing synechocystis sp. Strain pcc 6803 with N2 and CO2 in a diel regime reveals multiphase glycogen dynamics with low maintenance costs. Applied and Environmental Microbiology. 82(14), 4180–4189.
Angermayr, Andreas, et al. “Culturing Synechocystis Sp. Strain Pcc 6803 with N2 and CO2 in a Diel Regime Reveals Multiphase Glycogen Dynamics with Low Maintenance Costs.” Applied and Environmental Microbiology, vol. 82, no. 14, American Society for Microbiology, 2016, pp. 4180–89, doi:10.1128/AEM.00256-16.

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