Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp.   PCC 6803 Δ glg C , a strain incapable of glycogen storage

Carrieri, Damian; Broadbent, Charlie; Carruth, David; Paddock, Troy; Ungerer, Justin; Maness, Pin‐Ching; Ghirardi, Maria; Yu, Jianping

doi:10.1111/1751-7915.12243

Title: Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp. PCC 6803 Δ glg C , a strain incapable of glycogen storage

Abstract

We describe how a key objective in microbial biofuels strain development is to maximize carbon flux to target products while minimizing cell biomass accumulation, such that ideally the algae and bacteria would operate in a photo-catalytic state. A brief period of such a physiological state has recently been demonstrated in the cyanobacterium Synechocystis sp. PCC 6803 ΔglgC strain incapable of glycogen storage. When deprived of nitrogen, the ΔglgC excretes the organic acids alpha-ketoglutarate and pyruvate for a number of days without increasing cell biomass. This study examines the relationship between the growth state and the photo-catalytic state, and characterizes the metabolic adaptability of the photo-catalytic state to increasing light intensity. It is found that the culture can transition naturally from the growth state into the photo-catalytic state when provided with limited nitrogen supply during the growth phase. Photosynthetic capacity and pigments are lost over time in the photo-catalytic state. Reversal to growth state is observed with re-addition of nitrogen nutrient, accompanied by restoration of photosynthetic capacity and pigment levels in the cells. While the overall productivity increased under high light conditions, the ratio of alpha-ketoglutarate/pyruvate is altered, suggesting that carbon partition between the two products is adaptable to environmental conditions.

Authors:

Carrieri, Damian ^[1]; Broadbent, Charlie ^[1]; Carruth, David ^[1]; Paddock, Troy ^[1]; Ungerer, Justin ^[1]; Maness, Pin‐Ching ^[1]; Ghirardi, Maria ^[1]; Yu, Jianping ^[1]

Biosciences Center National Renewable Energy Laboratory 15013 Denver West Parkway Golden CO 80401 USA

Publication Date:: Fri Jan 23 00:00:00 EST 2015

Research Org.:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Hydrogen Fuel Cell Technologies Office (HFTO)

OSTI Identifier:: 1345698

Alternate Identifier(s):: OSTI ID: 1220612; OSTI ID: 1345699

Report Number(s):: NREL/JA-2700-62489
Journal ID: ISSN 1751-7915

Grant/Contract Number:: AC36-08GO28308

Resource Type:: Published Article

Journal Name:: Microbial Biotechnology (Online)

Additional Journal Information:: Journal Name: Microbial Biotechnology (Online) Journal Volume: 8 Journal Issue: 2; Journal ID: ISSN 1751-7915

Publisher:: Wiley-Blackwell

Country of Publication:: United Kingdom

Language:: English

Subject:: 09 BIOMASS FUELS; Synechocystis sp.; photo-catalysis, organic acids

Citation Formats


                    Carrieri, Damian, Broadbent, Charlie, Carruth, David, Paddock, Troy, Ungerer, Justin, Maness, Pin‐Ching, Ghirardi, Maria, and Yu, Jianping. Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp.   PCC 6803 Δ glg C , a strain incapable of glycogen storage.  United Kingdom: N. p., 2015. 
Web.  doi:10.1111/1751-7915.12243.

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                    Carrieri, Damian, Broadbent, Charlie, Carruth, David, Paddock, Troy, Ungerer, Justin, Maness, Pin‐Ching, Ghirardi, Maria, & Yu, Jianping. Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp.   PCC 6803 Δ glg C , a strain incapable of glycogen storage.  United Kingdom.  https://doi.org/10.1111/1751-7915.12243

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                    Carrieri, Damian, Broadbent, Charlie, Carruth, David, Paddock, Troy, Ungerer, Justin, Maness, Pin‐Ching, Ghirardi, Maria, and Yu, Jianping. Fri .  
"Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp.   PCC 6803 Δ glg C , a strain incapable of glycogen storage".  United Kingdom.  https://doi.org/10.1111/1751-7915.12243.

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@article{osti_1345698,

  title        = {Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp.   PCC 6803 Δ glg C , a strain incapable of glycogen storage},

  author       = {Carrieri, Damian and Broadbent, Charlie and Carruth, David and Paddock, Troy and Ungerer, Justin and Maness, Pin‐Ching and Ghirardi, Maria and Yu, Jianping},

  abstractNote = {We describe how a key objective in microbial biofuels strain development is to maximize carbon flux to target products while minimizing cell biomass accumulation, such that ideally the algae and bacteria would operate in a photo-catalytic state. A brief period of such a physiological state has recently been demonstrated in the cyanobacterium Synechocystis sp. PCC 6803 ΔglgC strain incapable of glycogen storage. When deprived of nitrogen, the ΔglgC excretes the organic acids alpha-ketoglutarate and pyruvate for a number of days without increasing cell biomass. This study examines the relationship between the growth state and the photo-catalytic state, and characterizes the metabolic adaptability of the photo-catalytic state to increasing light intensity. It is found that the culture can transition naturally from the growth state into the photo-catalytic state when provided with limited nitrogen supply during the growth phase. Photosynthetic capacity and pigments are lost over time in the photo-catalytic state. Reversal to growth state is observed with re-addition of nitrogen nutrient, accompanied by restoration of photosynthetic capacity and pigment levels in the cells. While the overall productivity increased under high light conditions, the ratio of alpha-ketoglutarate/pyruvate is altered, suggesting that carbon partition between the two products is adaptable to environmental conditions.},

  doi          = {10.1111/1751-7915.12243},

  journal      = {Microbial Biotechnology (Online)},

  number       = 2,

  volume       = 8,

  place        = {United Kingdom},

  year         = {Fri Jan 23 00:00:00 EST 2015},

  month        = {Fri Jan 23 00:00:00 EST 2015}

}

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Works referenced in this record:

Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803
journal, October 2012

Grundel, M.; Scheunemann, R.; Lockau, W.
Microbiology, Vol. 158, Issue Pt_12
DOI: 10.1099/mic.0.062950-0

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

Isobutanol production as an alternative metabolic sink to rescue the growth deficiency of the glycogen mutant of Synechococcus elongatus PCC 7942
journal, March 2014

Li, Xiaoqian; Shen, Claire R.; Liao, James C.
Photosynthesis Research, Vol. 120, Issue 3
DOI: 10.1007/s11120-014-9987-6

Rhythms in Energy Storage Control the Ability of the Cyanobacterial Circadian Clock to Reset
journal, August 2014

Pattanayak, Gopal K.; Phong, Connie; Rust, Michael J.
Current Biology, Vol. 24, Issue 16
DOI: 10.1016/j.cub.2014.07.022

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

Hickman, Jason W.; Kotovic, Kimberly M.; Miller, Cameron
Algal Research, Vol. 2, Issue 2
DOI: 10.1016/j.algal.2013.01.008

Aquatic phototrophs: efficient alternatives to land-based crops for biofuels
journal, June 2008

Dismukes, G. Charles; Carrieri, Damian; Bennette, Nicholas
Current Opinion in Biotechnology, Vol. 19, Issue 3
DOI: 10.1016/j.copbio.2008.05.007

Engineering cyanobacteria for the production of a cyclic hydrocarbon fuel from CO ₂ and H ₂ O
journal, January 2014

Halfmann, Charles; Gu, Liping; Zhou, Ruanbao
Green Chem., Vol. 16, Issue 6
DOI: 10.1039/C3GC42591F

Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production
journal, January 2012

Melis, Anastasios
Energy Environ. Sci., Vol. 5, Issue 2
DOI: 10.1039/C1EE02514G

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

Krasikov, Vladimir; Aguirre von Wobeser, Eneas; Dekker, Henk L.
Physiologia Plantarum, Vol. 145, Issue 3
DOI: 10.1111/j.1399-3054.2012.01585.x

Nitrogen Starvation-Induced Chlorosis in Synechococcus PCC 7942. Low-Level Photosynthesis As a Mechanism of Long-Term Survival
journal, May 2001

Sauer, Jörg; Schreiber, Ulrich; Schmid, Roland
Plant Physiology, Vol. 126, Issue 1
DOI: 10.1104/pp.126.1.233

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Similar Records

Title: Enhancing photo‐catalytic production of organic acids in the cyanobacterium S ynechocystis sp. PCC 6803 Δ glg C , a strain incapable of glycogen storage

Abstract

Citation Formats

Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803 journal, October 2012

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

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Rhythms in Energy Storage Control the Ability of the Cyanobacterial Circadian Clock to Reset journal, August 2014

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

Aquatic phototrophs: efficient alternatives to land-based crops for biofuels journal, June 2008

Engineering cyanobacteria for the production of a cyclic hydrocarbon fuel from CO 2 and H 2 O journal, January 2014

Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production journal, January 2012

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

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journal, June 2014

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journal, March 2014

Rhythms in Energy Storage Control the Ability of the Cyanobacterial Circadian Clock to Reset
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