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Title: Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway

Abstract

Carotenoids protect the photosynthetic apparatus against harmful radicals arising from the presence of both light and oxygen. They also act as accessory pigments for harvesting solar energy, and are required for stable assembly of many light-harvesting complexes. In the phototrophic bacterium Rhodobacter (Rba.) sphaeroides phytoene desaturase (CrtI) catalyses three sequential desaturations of the colourless carotenoid phytoene, extending the number of conjugated carbon-carbon double bonds, N, from three to nine and producing the yellow carotenoid neurosporene; subsequent modifications produce the yellow/red carotenoids spheroidene/spheroidenone (N=10/11). Genomic crtI replacements were used to swap the native three-step Rba. sphaeroides CrtI for the four-step Pantoea agglomerans enzyme, which re-routed carotenoid biosynthesis and culminated in the production of 2,2'-diketo-spirilloxanthin under semi-aerobic conditions. The new carotenoid pathway was elucidated using a combination of HPLC and mass spectrometry. Premature termination of this new pathway by inactivating crtC or crtD produced strains with lycopene or rhodopin as major carotenoids. All of the spirilloxanthin series carotenoids are accepted by the assembly pathways for LH2 and RC-LH1-PufX complexes. The efficiency of carotenoid-to-bacteriochlorophyll energy transfer for 2,2'-diketo-spirilloxanthin (15 conjugated CC bonds; N=15) in LH2 complexes is low, at 35%. High energy transfer efficiencies were obtained for neurosporene (N=9; 94%), spheroidene (N=10; 96%)more » and spheroidenone (N=11; 95%), whereas intermediate values were measured for lycopene (N=11; 64%), rhodopin (N=11; 62%) and spirilloxanthin (N=13; 39%). In conclusion, the variety and stability of these novel Rba. sphaeroides antenna complexes make them useful experimental models for investigating the energy transfer dynamics of carotenoids in bacterial photosynthesis.« less

Authors:
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Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Contributing Org.:
PARC partners with Washington University in St. Louis (lead); University of California, Riverside; University of Glasgow, UK; Los Alamos National Laboratory; University of New Mexico; New Mexico Corsortium; North Carolina State University; Northwestern University; Oak Ridge National Laboratory; University of Pennsylvania; Sandia National Laboratories; University of Sheffield, UK
OSTI Identifier:
1233984
Alternate Identifier(s):
OSTI ID: 1168386
Grant/Contract Number:  
SC0001035; 8P41GM103422-35; EP/I012060/1; BB/G021546/1; 338895
Resource Type:
Journal Article: Published Article
Journal Name:
Biochimica et Biophysica Acta - Bioenergetics
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1847 Journal Issue: 2; Journal ID: ISSN 0005-2728
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; solar (fuels); photosynthesis (natural and artificial); biofuels (including algae and biomass); bio-inspired; charge transport; membrane; synthesis (novel materials); synthesis (self-assembly); Bacterial photosynthesis; Light harvesting; Carotenoid; Membrane protein; Antenna; Synthetic biology

Citation Formats

Chi, Shuang C., Mothersole, David J., Dilbeck, Preston, Niedzwiedzki, Dariusz M., Zhang, Hao, Qian, Pu, Vasilev, Cvetelin, Grayson, Katie J., Jackson, Philip J., Martin, Elizabeth C., Li, Ying, Holten, Dewey, and Neil Hunter, C. Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway. Netherlands: N. p., 2015. Web. doi:10.1016/j.bbabio.2014.10.004.
Chi, Shuang C., Mothersole, David J., Dilbeck, Preston, Niedzwiedzki, Dariusz M., Zhang, Hao, Qian, Pu, Vasilev, Cvetelin, Grayson, Katie J., Jackson, Philip J., Martin, Elizabeth C., Li, Ying, Holten, Dewey, & Neil Hunter, C. Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway. Netherlands. https://doi.org/10.1016/j.bbabio.2014.10.004
Chi, Shuang C., Mothersole, David J., Dilbeck, Preston, Niedzwiedzki, Dariusz M., Zhang, Hao, Qian, Pu, Vasilev, Cvetelin, Grayson, Katie J., Jackson, Philip J., Martin, Elizabeth C., Li, Ying, Holten, Dewey, and Neil Hunter, C. Sun . "Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway". Netherlands. https://doi.org/10.1016/j.bbabio.2014.10.004.
@article{osti_1233984,
title = {Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway},
author = {Chi, Shuang C. and Mothersole, David J. and Dilbeck, Preston and Niedzwiedzki, Dariusz M. and Zhang, Hao and Qian, Pu and Vasilev, Cvetelin and Grayson, Katie J. and Jackson, Philip J. and Martin, Elizabeth C. and Li, Ying and Holten, Dewey and Neil Hunter, C.},
abstractNote = {Carotenoids protect the photosynthetic apparatus against harmful radicals arising from the presence of both light and oxygen. They also act as accessory pigments for harvesting solar energy, and are required for stable assembly of many light-harvesting complexes. In the phototrophic bacterium Rhodobacter (Rba.) sphaeroides phytoene desaturase (CrtI) catalyses three sequential desaturations of the colourless carotenoid phytoene, extending the number of conjugated carbon-carbon double bonds, N, from three to nine and producing the yellow carotenoid neurosporene; subsequent modifications produce the yellow/red carotenoids spheroidene/spheroidenone (N=10/11). Genomic crtI replacements were used to swap the native three-step Rba. sphaeroides CrtI for the four-step Pantoea agglomerans enzyme, which re-routed carotenoid biosynthesis and culminated in the production of 2,2'-diketo-spirilloxanthin under semi-aerobic conditions. The new carotenoid pathway was elucidated using a combination of HPLC and mass spectrometry. Premature termination of this new pathway by inactivating crtC or crtD produced strains with lycopene or rhodopin as major carotenoids. All of the spirilloxanthin series carotenoids are accepted by the assembly pathways for LH2 and RC-LH1-PufX complexes. The efficiency of carotenoid-to-bacteriochlorophyll energy transfer for 2,2'-diketo-spirilloxanthin (15 conjugated CC bonds; N=15) in LH2 complexes is low, at 35%. High energy transfer efficiencies were obtained for neurosporene (N=9; 94%), spheroidene (N=10; 96%) and spheroidenone (N=11; 95%), whereas intermediate values were measured for lycopene (N=11; 64%), rhodopin (N=11; 62%) and spirilloxanthin (N=13; 39%). In conclusion, the variety and stability of these novel Rba. sphaeroides antenna complexes make them useful experimental models for investigating the energy transfer dynamics of carotenoids in bacterial photosynthesis.},
doi = {10.1016/j.bbabio.2014.10.004},
url = {https://www.osti.gov/biblio/1233984}, journal = {Biochimica et Biophysica Acta - Bioenergetics},
issn = {0005-2728},
number = 2,
volume = 1847,
place = {Netherlands},
year = {2015},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1016/j.bbabio.2014.10.004

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Cited by: 23 works
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Works referencing / citing this record:

Rhodobacter thermarum sp. nov., a novel phototrophic bacterium isolated from sediment of a hot spring
journal, February 2019


Carotenoid-to-(bacterio)chlorophyll energy transfer in LH2 antenna complexes from Rba. sphaeroides reconstituted with non-native (bacterio)chlorophylls
journal, July 2019


Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre
journal, January 2017


Light harvesting in phototrophic bacteria: structure and function
journal, June 2017


A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria
journal, August 2018