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Title: Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage

Abstract

Molecular mechanisms that regulate carbon flux are poorly understood in algae. The ΔglgC mutant of the cyanobacterium Synechocystis sp. PCC 6803 is incapable of glycogen storage and displays an array of physiological responses under nitrogen starvation that are different from wild-type (WT). These include non-bleaching phenotype and the redirection of photosynthetically fixed carbon towards excreted organic acids (overflow metabolism) without biomass growth. To understand the role of gene/protein expression in these responses, we followed the time course of transcripts by genome-scale microarrays and proteins by shotgun proteomics in ΔglgC and WT cells upon nitrogen starvation. Compared to WT, the degradation of phycobilisome rod proteins was delayed and attenuated in the mutant, and the core proteins were less degraded; both contributed to the non-bleaching appearance despite the induction of nblA genes, suggesting the presence of a break in regulation of the phycobilisome degradation pathway downstream of nblA induction. The mutant displayed NtcA-mediated transcriptional response to nitrogen starvation, indicating that it is able to sense nitrogen status. Furthermore, some responses to nitrogen starvation appear to be stronger in the mutant, as shown by the increases in transcripts for the transcriptional regulator, rre37, which regulates central carbon metabolism. Accordingly, multiple proteins involved inmore » photosynthesis, central carbon metabolism, and carbon storage and utilization showed lower abundance in the mutant. Furthermore, these results indicate that the transition in the central carbon metabolism from growth to overflow metabolism in ΔglgC does not require increases in expression of the overflow pathway enzymes; the transition and non-bleaching phenotype are likely regulated instead at the metabolite level.« less

Authors:
 [1];  [2];  [1];  [3];  [2];  [3];  [4];  [3];  [3];  [3];  [3]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States); Matrix Genetics, LLC, Seattle, WA (United States)
  2. Washington and Jefferson College, Washington, PA (United States)
  3. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  4. Univ. of Colorado, Boulder, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1335210
Alternate Identifier(s):
OSTI ID: 1396618
Report Number(s):
NREL/JA-2700-65975
Journal ID: ISSN 2211-9264
Grant/Contract Number:  
AC36-08GO28308; FWP ERWER0A; AC36-08-GO28308
Resource Type:
Accepted Manuscript
Journal Name:
Algal Research
Additional Journal Information:
Journal Volume: 21; Journal Issue: C; Journal ID: ISSN 2211-9264
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; algae; cyanobacterium; glycogen storage; nitrogen starvation

Citation Formats

Carrieri, Damian, Lombardi, Thomas, Paddock, Troy, Cano, Melissa, Goodney, Gabriel A., Nag, Ambarish, Old, William, Maness, Pin -Ching, Seibert, Michael, Ghirardi, Maria, and Yu, Jianping. Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage. United States: N. p., 2016. Web. https://doi.org/10.1016/j.algal.2016.11.003.
Carrieri, Damian, Lombardi, Thomas, Paddock, Troy, Cano, Melissa, Goodney, Gabriel A., Nag, Ambarish, Old, William, Maness, Pin -Ching, Seibert, Michael, Ghirardi, Maria, & Yu, Jianping. Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage. United States. https://doi.org/10.1016/j.algal.2016.11.003
Carrieri, Damian, Lombardi, Thomas, Paddock, Troy, Cano, Melissa, Goodney, Gabriel A., Nag, Ambarish, Old, William, Maness, Pin -Ching, Seibert, Michael, Ghirardi, Maria, and Yu, Jianping. Thu . "Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage". United States. https://doi.org/10.1016/j.algal.2016.11.003. https://www.osti.gov/servlets/purl/1335210.
@article{osti_1335210,
title = {Transcriptome and proteome analysis of nitrogen starvation responses in Synechocystis 6803 ΔglgC, a mutant incapable of glycogen storage},
author = {Carrieri, Damian and Lombardi, Thomas and Paddock, Troy and Cano, Melissa and Goodney, Gabriel A. and Nag, Ambarish and Old, William and Maness, Pin -Ching and Seibert, Michael and Ghirardi, Maria and Yu, Jianping},
abstractNote = {Molecular mechanisms that regulate carbon flux are poorly understood in algae. The ΔglgC mutant of the cyanobacterium Synechocystis sp. PCC 6803 is incapable of glycogen storage and displays an array of physiological responses under nitrogen starvation that are different from wild-type (WT). These include non-bleaching phenotype and the redirection of photosynthetically fixed carbon towards excreted organic acids (overflow metabolism) without biomass growth. To understand the role of gene/protein expression in these responses, we followed the time course of transcripts by genome-scale microarrays and proteins by shotgun proteomics in ΔglgC and WT cells upon nitrogen starvation. Compared to WT, the degradation of phycobilisome rod proteins was delayed and attenuated in the mutant, and the core proteins were less degraded; both contributed to the non-bleaching appearance despite the induction of nblA genes, suggesting the presence of a break in regulation of the phycobilisome degradation pathway downstream of nblA induction. The mutant displayed NtcA-mediated transcriptional response to nitrogen starvation, indicating that it is able to sense nitrogen status. Furthermore, some responses to nitrogen starvation appear to be stronger in the mutant, as shown by the increases in transcripts for the transcriptional regulator, rre37, which regulates central carbon metabolism. Accordingly, multiple proteins involved in photosynthesis, central carbon metabolism, and carbon storage and utilization showed lower abundance in the mutant. Furthermore, these results indicate that the transition in the central carbon metabolism from growth to overflow metabolism in ΔglgC does not require increases in expression of the overflow pathway enzymes; the transition and non-bleaching phenotype are likely regulated instead at the metabolite level.},
doi = {10.1016/j.algal.2016.11.003},
journal = {Algal Research},
number = C,
volume = 21,
place = {United States},
year = {2016},
month = {11}
}

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Works referenced in this record:

Energy biotechnology with cyanobacteria
journal, June 2009

  • Angermayr, S. Andreas; Hellingwerf, Klaas J.; Lindblad, Peter
  • Current Opinion in Biotechnology, Vol. 20, Issue 3, p. 257-263
  • DOI: 10.1016/j.copbio.2009.05.011

Engineering cyanobacteria to generate high-value products
journal, February 2011


Glycogen synthesis is a required component of the nitrogen stress response in Synechococcus elongatus PCC 7942
journal, March 2013


Photo-catalytic conversion of carbon dioxide to organic acids by a recombinant cyanobacterium incapable of glycogen storage
journal, January 2012

  • Carrieri, Damian; Paddock, Troy; Maness, Pin-Ching
  • Energy & Environmental Science, Vol. 5, Issue 11, p. 9457-9461
  • DOI: 10.1039/c2ee23181f

Time-series resolution of gradual nitrogen starvation and its impact on photosynthesis in the cyanobacterium Synechocystis PCC 6803
journal, March 2012


Global Proteomics Reveal an Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations
journal, September 2010

  • Wegener, Kimberly M.; Singh, Abhay K.; Jacobs, Jon M.
  • Molecular & Cellular Proteomics, Vol. 9, Issue 12
  • DOI: 10.1074/mcp.M110.000109

Dynamics of Photosynthesis in a Glycogen-Deficient glgC Mutant of Synechococcus sp. Strain PCC 7002
journal, September 2015

  • Jackson, Simon A.; Eaton-Rye, Julian J.; Bryant, Donald A.
  • Applied and Environmental Microbiology, Vol. 81, Issue 18
  • DOI: 10.1128/AEM.01751-15

Identification and quantification of water-soluble metabolites by cryoprobe-assisted nuclear magnetic resonance spectroscopy applied to microbial fermentation
journal, May 2009

  • Carrieri, Damian; McNeely, Kelsey; De Roo, Ana C.
  • Magnetic Resonance in Chemistry, Vol. 47, Issue S1
  • DOI: 10.1002/mrc.2420

IsoformResolver: A Peptide-Centric Algorithm for Protein Inference
journal, July 2011

  • Meyer-Arendt, Karen; Old, William M.; Houel, Stephane
  • Journal of Proteome Research, Vol. 10, Issue 7
  • DOI: 10.1021/pr200039p

Comparison of Label-free Methods for Quantifying Human Proteins by Shotgun Proteomics
journal, June 2005

  • Old, William M.; Meyer-Arendt, Karen; Aveline-Wolf, Lauren
  • Molecular & Cellular Proteomics, Vol. 4, Issue 10
  • DOI: 10.1074/mcp.M500084-MCP200

Decomposition of Gene Expression State Space Trajectories
journal, December 2009


Significance analysis of time course microarray experiments
journal, September 2005

  • Storey, J. D.; Xiao, W.; Leek, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 36
  • DOI: 10.1073/pnas.0504609102

Engineering Limonene and Bisabolene Production in Wild Type and a Glycogen-Deficient Mutant of Synechococcus sp. PCC 7002
journal, June 2014

  • Davies, Fiona K.; Work, Victoria H.; Beliaev, Alexander S.
  • Frontiers in Bioengineering and Biotechnology, Vol. 2
  • DOI: 10.3389/fbioe.2014.00021

Sll1330 controls the expression of glycolytic genes in Synechocystis sp. PCC 6803
journal, April 2007

  • Tabei, Yosuke; Okada, Katsuhiko; Tsuzuki, Mikio
  • Biochemical and Biophysical Research Communications, Vol. 355, Issue 4
  • DOI: 10.1016/j.bbrc.2007.02.065

A Response Regulator Rre37 and an RNA Polymerase Sigma Factor SigE Represent Two Parallel Pathways to Activate Sugar Catabolism in a Cyanobacterium Synechocystis sp. PCC 6803
journal, January 2011

  • Azuma, Miyuki; Osanai, Takashi; Hirai, Masami Yokota
  • Plant and Cell Physiology, Vol. 52, Issue 2
  • DOI: 10.1093/pcp/pcq204

Two Regulatory Networks Mediated by Light and Glucose Involved in Glycolytic Gene Expression in Cyanobacteria
journal, August 2012

  • Tabei, Yosuke; Okada, Katsuhiko; Horii, Eisuke
  • Plant and Cell Physiology, Vol. 53, Issue 10
  • DOI: 10.1093/pcp/pcs115

rre37 Overexpression Alters Gene Expression Related to the Tricarboxylic Acid Cycle and Pyruvate Metabolism in Synechocystis sp. PCC 6803
journal, January 2014

  • Iijima, Hiroko; Watanabe, Atsuko; Takanobu, Junko
  • The Scientific World Journal, Vol. 2014
  • DOI: 10.1155/2014/921976

Rre37 stimulates accumulation of 2-oxoglutarate and glycogen under nitrogen starvation in Synechocystis sp. PCC 6803
journal, December 2013


Cyanobacteria Perceive Nitrogen Status by Sensing Intracellular 2-Oxoglutarate Levels
journal, October 2001

  • Muro-Pastor, M. Isabel; Reyes, José C.; Florencio, Francisco J.
  • Journal of Biological Chemistry, Vol. 276, Issue 41
  • DOI: 10.1074/jbc.M105297200

Functions of the Duplicated hik31 Operons in Central Metabolism and Responses to Light, Dark, and Carbon Sources in Synechocystis sp. Strain PCC 6803
journal, January 2012

  • Nagarajan, Sowmya; Sherman, Debra M.; Shaw, Isaac
  • Journal of Bacteriology, Vol. 194, Issue 2
  • DOI: 10.1128/JB.06207-11

Essential role of the plasmid hik31 operon in regulating central metabolism in the dark in Synechocystis sp. PCC 6803: P3 regulates dark growth and metabolism
journal, November 2013

  • Nagarajan, Sowmya; Srivastava, Sanvesh; Sherman, Louis A.
  • Molecular Microbiology, Vol. 91, Issue 1
  • DOI: 10.1111/mmi.12442

A putative sensor kinase, Hik31, is involved in the response of Synechocystis sp. strain PCC 6803 to the presence of glucose
journal, March 2006

  • Kahlon, Shira; Beeri, Karen; Ohkawa, Hiroshi
  • Microbiology, Vol. 152, Issue 3
  • DOI: 10.1099/mic.0.28510-0

Differential Gene Expression in Response to Hydrogen Peroxide and the Putative PerR Regulon of Synechocystis sp. Strain PCC 6803
journal, May 2004


A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions
journal, September 1998

  • Schwarz, R.; Grossman, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 18
  • DOI: 10.1073/pnas.95.18.11008

The role of the bidirectional hydrogenase in cyanobacteria
journal, September 2011


Identification of hox genes and analysis of their transcription in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 growing under nitrate-limiting conditions
journal, September 2002


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    journal, January 2019

    • Wang, Yiming; Ma, Chen; Zhang, Jin
    • Analytical Methods, Vol. 11, Issue 33
    • DOI: 10.1039/c9ay00406h

    In silico strategies to couple production of bioethanol with growth in cyanobacteria
    journal, May 2019

    • Lasry Testa, Romina; Delpino, Claudio; Estrada, Vanina
    • Biotechnology and Bioengineering, Vol. 116, Issue 8
    • DOI: 10.1002/bit.26998