Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance
Abstract
Genetic engineering of photosynthetic organisms typically redirects native metabolism towards desirable products, which thereby represent new metabolic sinks. There is limited information on how these modifications impact the evolved mechanisms of photosynthetic energy metabolism and cellular growth. Two engineered strains of Synechocystis sp. PCC 6803 with altered carbon sink capacity were assayed for their photosynthetic and CO2 concentrating mechanism properties in conditions of high and low inorganic carbon (Ci) availability. In the ΔglgC mutant, glycogen cannot be synthesized and a carbon sink pathway has been effectively removed. The JU547 strain has been engineered by integration of the Pseudomonas syringae ethylene forming enzyme and provides a new sink. When cultured under high carbon conditions, ΔglgC displayed diminished photochemical efficiency, a more reduced NADPH pool, delayed initiation of the Calvin-Benson-Bassham cycle, and impairment of linear and cyclic electron flows. It also exhibited a large decrease in photochemical quenching indicative of the accumulation of QA-, normally associated with a reduced PQ pool, but appears instead to be the result of an undefined dissipative mechanism to spill excess energy. In the case of carbon sink integration, JU547 displayed slightly more oxidized PQ and NADPH pools and increased rates of cyclic electron flow and anmore »
- Authors:
-
- Oklahoma State Univ., Stillwater, OK (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office; USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1330802
- Alternate Identifier(s):
- OSTI ID: 1396394
- Report Number(s):
- NREL/JA-2700-66083
Journal ID: ISSN 2211-9264
- Grant/Contract Number:
- AC36-08GO28308; FG02-08ER15968; FWP ERWER0A
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Algal Research
- Additional Journal Information:
- Journal Volume: 20; Journal Issue: C; Journal ID: ISSN 2211-9264
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; chlorophyll fluorescence; cyclic electron flow; ethylene; glycogen; homeostasis; metabolic sink; NADPH; photosystem; plastoquinone
Citation Formats
Holland, Steven C., Artier, Juliana, Miller, Neil T., Cano, Melissa, Yu, Jianping, Ghirardi, Maria L., and Burnap, Robert L. Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance. United States: N. p., 2016.
Web. doi:10.1016/j.algal.2016.09.021.
Holland, Steven C., Artier, Juliana, Miller, Neil T., Cano, Melissa, Yu, Jianping, Ghirardi, Maria L., & Burnap, Robert L. Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance. United States. https://doi.org/10.1016/j.algal.2016.09.021
Holland, Steven C., Artier, Juliana, Miller, Neil T., Cano, Melissa, Yu, Jianping, Ghirardi, Maria L., and Burnap, Robert L. Wed .
"Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance". United States. https://doi.org/10.1016/j.algal.2016.09.021. https://www.osti.gov/servlets/purl/1330802.
@article{osti_1330802,
title = {Impacts of genetically engineered alterations in carbon sink pathways on photosynthetic performance},
author = {Holland, Steven C. and Artier, Juliana and Miller, Neil T. and Cano, Melissa and Yu, Jianping and Ghirardi, Maria L. and Burnap, Robert L.},
abstractNote = {Genetic engineering of photosynthetic organisms typically redirects native metabolism towards desirable products, which thereby represent new metabolic sinks. There is limited information on how these modifications impact the evolved mechanisms of photosynthetic energy metabolism and cellular growth. Two engineered strains of Synechocystis sp. PCC 6803 with altered carbon sink capacity were assayed for their photosynthetic and CO2 concentrating mechanism properties in conditions of high and low inorganic carbon (Ci) availability. In the ΔglgC mutant, glycogen cannot be synthesized and a carbon sink pathway has been effectively removed. The JU547 strain has been engineered by integration of the Pseudomonas syringae ethylene forming enzyme and provides a new sink. When cultured under high carbon conditions, ΔglgC displayed diminished photochemical efficiency, a more reduced NADPH pool, delayed initiation of the Calvin-Benson-Bassham cycle, and impairment of linear and cyclic electron flows. It also exhibited a large decrease in photochemical quenching indicative of the accumulation of QA-, normally associated with a reduced PQ pool, but appears instead to be the result of an undefined dissipative mechanism to spill excess energy. In the case of carbon sink integration, JU547 displayed slightly more oxidized PQ and NADPH pools and increased rates of cyclic electron flow and an enhanced demand for inorganic carbon as suggested by increase in the expression of the bicarbonate transporter, SbtA. Overall, the results highlight the importance of the native regulatory network of autotrophic metabolism in governing photosynthetic performance and provide cogent examples of both predicable and difficult to predict phenotypic consequences upon installation of new pathways in autotrophs.},
doi = {10.1016/j.algal.2016.09.021},
journal = {Algal Research},
number = C,
volume = 20,
place = {United States},
year = {Wed Oct 05 00:00:00 EDT 2016},
month = {Wed Oct 05 00:00:00 EDT 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 14 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Metabolic design for cyanobacterial chemical synthesis
journal, April 2014
- Oliver, John W. K.; Atsumi, Shota
- Photosynthesis Research, Vol. 120, Issue 3
Engineering cyanobacteria as photosynthetic feedstock factories
journal, February 2014
- Hays, Stephanie G.; Ducat, Daniel C.
- Photosynthesis Research, Vol. 123, Issue 3
Metabolic engineering of cyanobacteria for the synthesis of commodity products
journal, June 2015
- Angermayr, S. Andreas; Gorchs Rovira, Aleix; Hellingwerf, Klaas J.
- Trends in Biotechnology, Vol. 33, Issue 6
A carbon sink pathway increases carbon productivity in cyanobacteria
journal, May 2015
- Oliver, John W. K.; Atsumi, Shota
- Metabolic Engineering, Vol. 29
Predicting Dissolved Inorganic Carbon in Photoautotrophic Microalgae Culture via the Nitrogen Source
journal, August 2015
- Nguyen, Binh T.; Rittmann, Bruce E.
- Environmental Science & Technology, Vol. 49, Issue 16
Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria
journal, May 1998
- Ibelings, Bas W.; Maberly, Stephen C.
- Limnology and Oceanography, Vol. 43, Issue 3
Rising CO2 Levels Will Intensify Phytoplankton Blooms in Eutrophic and Hypertrophic Lakes
journal, August 2014
- Verspagen, Jolanda M. H.; Van de Waal, Dedmer B.; Finke, Jan F.
- PLoS ONE, Vol. 9, Issue 8
Enhanced biological carbon consumption in a high CO2 ocean
journal, November 2007
- Riebesell, U.; Schulz, K. G.; Bellerby, R. G. J.
- Nature, Vol. 450, Issue 7169
Phycobilisome-Deficient Strains of Synechocystis sp. PCC 6803 Have Reduced Size and Require Carbon-Limiting Conditions to Exhibit Enhanced Productivity
journal, April 2014
- Lea-Smith, David J.; Bombelli, Paolo; Dennis, John S.
- Plant Physiology, Vol. 165, Issue 2
Installing extra bicarbonate transporters in the cyanobacterium Synechocystis sp. PCC6803 enhances biomass production
journal, May 2015
- Kamennaya, Nina A.; Ahn, SeEun; Park, Hanwool
- Metabolic Engineering, Vol. 29
Regulation of CO2 Concentrating Mechanism in Cyanobacteria
journal, January 2015
- Burnap, Robert; Hagemann, Martin; Kaplan, Aaron
- Life, Vol. 5, Issue 1
Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants
journal, June 2007
- Price, G. Dean; Badger, Murray R.; Woodger, Fiona J.
- Journal of Experimental Botany, Vol. 59, Issue 7
Protein-based organelles in bacteria: carboxysomes and related microcompartments
journal, August 2008
- Yeates, Todd O.; Kerfeld, Cheryl A.; Heinhorst, Sabine
- Nature Reviews Microbiology, Vol. 6, Issue 9
The Importance of Energy Balance in Improving Photosynthetic Productivity
journal, November 2010
- Kramer, David M.; Evans, John R.
- Plant Physiology, Vol. 155, Issue 1
Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions
journal, January 2010
- Alric, Jean; Lavergne, Jérôme; Rappaport, Fabrice
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 1
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
Sustained photosynthetic conversion of CO2 to ethylene in recombinant cyanobacterium Synechocystis 6803
journal, January 2012
- Ungerer, Justin; Tao, Ling; Davis, Mark
- Energy & Environmental Science, Vol. 5, Issue 10, p. 8998-9006
Succinate Dehydrogenase and Other Respiratory Pathways in Thylakoid Membranes of Synechocystis sp. Strain PCC 6803: Capacity Comparisons and Physiological Function
journal, July 2001
- Cooley, J. W.; Vermaas, W. F. J.
- Journal of Bacteriology, Vol. 183, Issue 14
The plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene
journal, April 2015
- Xiong, Wei; Morgan, John A.; Ungerer, Justin
- Nature Plants, Vol. 1, Issue 5
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates
journal, March 1968
- Allen, Mary Mennes
- Journal of Phycology, Vol. 4, Issue 1
Alterations in Global Patterns of Gene Expression in Synechocystis sp. PCC 6803 in Response to Inorganic Carbon Limitation and the Inactivation of ndhR , a LysR Family Regulator
journal, November 2003
- Wang, Hong-Liang; Postier, Bradley L.; Burnap, Robert L.
- Journal of Biological Chemistry, Vol. 279, Issue 7
[85] Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803
book, January 1988
- Williams, John G. K.
- Methods in Enzymology
Consistent Sets of Spectrophotometric Chlorophyll Equations for Acetone, Methanol and Ethanol Solvents
journal, June 2006
- Ritchie, Raymond J.
- Photosynthesis Research, Vol. 89, Issue 1
Metabolic and photosynthetic consequences of blocking starch biosynthesis in the green alga Chlamydomonas reinhardtii sta6 mutant
journal, March 2015
- Krishnan, Anagha; Kumaraswamy, G. Kenchappa; Vinyard, David J.
- The Plant Journal, Vol. 81, Issue 6
Respiration accumulates Calvin cycle intermediates for the rapid start of photosynthesis in Synechocystis sp. PCC 6803
journal, August 2014
- Shimakawa, Ginga; Hasunuma, Tomohisa; Kondo, Akihiko
- Bioscience, Biotechnology, and Biochemistry, Vol. 78, Issue 12
Effects of Inorganic Carbon Limitation on the Metabolome of the Synechocystis sp. PCC 6803 Mutant Defective in glnB Encoding the Central Regulator PII of Cyanobacterial C/N Acclimation
journal, April 2014
- Schwarz, Doreen; Orf, Isabel; Kopka, Joachim
- Metabolites, Vol. 4, Issue 2
Low-carbon acclimation in carboxysome-less and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803
journal, February 2012
- Hackenberg, Claudia; Huege, Jan; Engelhardt, Annerose
- Microbiology, Vol. 158, Issue 2
Genes Encoding A-Type Flavoproteins Are Essential for Photoreduction of O2 in Cyanobacteria
journal, February 2003
- Helman, Yael; Tchernov, Dan; Reinhold, Leonora
- Current Biology, Vol. 13, Issue 3, p. 230-235
Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light
journal, February 2013
- Allahverdiyeva, Y.; Mustila, H.; Ermakova, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 10
Redox changes accompanying inorganic carbon limitation in Synechocystis sp. PCC 6803
journal, March 2015
- Holland, Steven C.; Kappell, Anthony D.; Burnap, Robert L.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 3
On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient
journal, July 2011
- Stirbet, Alexandrina
- Journal of Photochemistry and Photobiology B: Biology, Vol. 104, Issue 1-2
A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts
journal, October 1979
- Briantais, J. -M.; Vernotte, C.; Picaud, M.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 548, Issue 1
The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition
journal, August 2012
- Kaňa, Radek; Kotabová, Eva; Komárek, Ondřej
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
Chlorophyll Fluorescence Analysis of Cyanobacterial Photosynthesis and Acclimation
journal, September 1998
- Campbell, Douglas; Hurry, Vaughan; Clarke, Adrian K.
- Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3
Chlorophyll a Fluorescence Yield as a Monitor of Both Active CO 2 and HCO 3 − Transport by the Cyanobacterium Synechococcus UTEX 625
journal, March 1988
- Miller, Anthony G.; Espie, George S.; Canvin, David T.
- Plant Physiology, Vol. 86, Issue 3
Effects of inorganic carbon accumulation on photosynthetic oxygen reduction and cyclic electron flow in the cyanobacterium Synechococcus PCC7942
journal, September 1993
- Badger, Murray R.; Schreiber, Ulrich
- Photosynthesis Research, Vol. 37, Issue 3
Photosystem activity and state transitions of the photosynthetic apparatus in cyanobacterium Synechocystis PCC 6803 mutants with different redox state of the plastoquinone pool
journal, January 2015
- Bolychevtseva, Y. V.; Kuzminov, F. I.; Elanskaya, I. V.
- Biochemistry (Moscow), Vol. 80, Issue 1
Characterization of the non-photochemical quenching of chlorophyll fluorescence that occurs during the active accumulation of inorganic carbon in the cyanobacterium Synechococcus PCC 7942
journal, September 1996
- Miller, Anthony G.; Espie, George S.; Bruce, Doug
- Photosynthesis Research, Vol. 49, Issue 3
Light-Induced Dynamic Changes of NADPH Fluorescence in Synechocystis PCC 6803 and Its ndhB-Defective Mutant M55
journal, October 2000
- Mi, Hualing; Klughammer, Christof; Schreiber, Ulrich
- Plant and Cell Physiology, Vol. 41, Issue 10
NADPH fluorescence in the cyanobacterium Synechocystis sp. PCC 6803: A versatile probe for in vivo measurements of rates, yields and pools
journal, June 2014
- Kauny, Jocelyn; Sétif, Pierre
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 6
Regulation of the Cyanobacterial CO2-Concentrating Mechanism Involves Internal Sensing of NADP+ and α-Ketogutarate Levels by Transcription Factor CcmR
journal, July 2012
- Daley, Shawn M. E.; Kappell, Anthony D.; Carrick, Marla J.
- PLoS ONE, Vol. 7, Issue 7
Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress
journal, January 2001
- Figge, R. M.; Cassier-Chauvat, C.; Chauvat, F.
- Molecular Microbiology, Vol. 39, Issue 2
Changes in photosynthesis and pigmentation in an agp deletion mutant of the cyanobacterium Synechocystis sp.
journal, January 2003
- Miao, Xiaoling; Wu, Qingyu; Wu, Guifang
- Biotechnology Letters, Vol. 25, Issue 5, p. 391-396
Reduction-Induced Suppression of Electron Flow (RISE) in the Photosynthetic Electron Transport System of Synechococcus elongatus PCC 7942
journal, December 2015
- Shaku, Keiichiro; Shimakawa, Ginga; Hashiguchi, Masaki
- Plant and Cell Physiology
Flavodiiron Protein Flv2/Flv4-Related Photoprotective Mechanism Dissipates Excitation Pressure of PSII in Cooperation with Phycobilisomes in Cyanobacteria
journal, December 2013
- Bersanini, Luca; Battchikova, Natalia; Jokel, Martina
- Plant Physiology, Vol. 164, Issue 2
Oxygenic photosynthesis-specific subunits of cyanobacterial NADPH dehydrogenases: Oxygenic Photosynthesis-Specific NDH-1 Subunit
journal, January 2015
- Ma, Weimin; Ogawa, Teruo
- IUBMB Life, Vol. 67, Issue 1
Altered carbohydrate metabolism in glycogen synthase mutants of Synechococcus sp. strain PCC 7002: Cell factories for soluble sugars
journal, March 2013
- Xu, Yu; Tiago Guerra, L.; Li, Zhongkui
- Metabolic Engineering, Vol. 16
Metabolome Phenotyping of Inorganic Carbon Limitation in Cells of the Wild Type and Photorespiratory Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803
journal, October 2008
- Eisenhut, Marion; Huege, Jan; Schwarz, Doreen
- Plant Physiology, Vol. 148, Issue 4
Works referencing / citing this record:
Membrane-Inlet Mass Spectrometry Enables a Quantitative Understanding of Inorganic Carbon Uptake Flux and Carbon Concentrating Mechanisms in Metabolically Engineered Cyanobacteria
journal, June 2019
- Douchi, Damien; Liang, Feiyan; Cano, Melissa
- Frontiers in Microbiology, Vol. 10
Lethality caused by ADP-glucose accumulation is suppressed by salt-induced carbon flux redirection in cyanobacteria
journal, December 2019
- Díaz-Troya, Sandra; Roldán, Miguel; Mallén-Ponce, Manuel J.
- Journal of Experimental Botany, Vol. 71, Issue 6
Recent advances in synthetic biology of cyanobacteria
journal, May 2018
- Sengupta, Annesha; Pakrasi, Himadri B.; Wangikar, Pramod P.
- Applied Microbiology and Biotechnology, Vol. 102, Issue 13
Membrane-Inlet Mass Spectrometry Enables a Quantitative Understanding of Inorganic Carbon Uptake Flux and Carbon Concentrating Mechanisms in Metabolically Engineered Cyanobacteria
journal, June 2019
- Douchi, Damien; Liang, Feiyan; Cano, Melissa
- Frontiers in Microbiology, Vol. 10