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Title: Phycobilisomes Harbor FNR L in Cyanobacteria

Abstract

ABSTRACT Cyanobacterial phycobilisomes (PBSs) are photosynthetic antenna complexes that harvest light energy and supply it to two reaction centers (RCs) where photochemistry starts. PBSs can be classified into two types, depending on the presence of allophycocyanin (APC): CpcG-PBS and CpcL-PBS. Because the accurate protein composition of CpcL-PBS remains unclear, we describe here its isolation and characterization from the cyanobacterium Synechocystis sp. strain 6803. We found that ferredoxin-NADP + oxidoreductase (or FNR L ), an enzyme involved in both cyclic electron transport and the terminal step of the electron transport chain in oxygenic photosynthesis, is tightly associated with CpcL-PBS as well as with CpcG-PBS. Room temperature and low-temperature fluorescence analyses show a red-shifted emission at 669 nm in CpcL-PBS as a terminal energy emitter without APC. SDS-PAGE and quantitative mass spectrometry reveal an increased content of FNR L and CpcC2, a rod linker protein, in CpcL-PBS compared to that of CpcG-PBS rods, indicative of an elongated CpcL-PBS rod length and its potential functional differences from CpcG-PBS. Furthermore, we combined isotope-encoded cross-linking mass spectrometry with computational protein structure predictions and structural modeling to produce an FNR L -PBS binding model that is supported by two cross-links between K 69 of FNR L andmore » the N terminus of CpcB, one component in PBS, in both CpcG-PBS and CpcL-PBS (cross-link 1), and between the N termini of FNR L and CpcB (cross-link 2). Our data provide a novel functional assembly form of phycobiliproteins and a molecular-level description of the close association of FNR L with phycocyanin in both CpcG-PBS and CpcL-PBS. IMPORTANCE Cyanobacterial light-harvesting complex PBSs are essential for photochemistry in light reactions and for balancing energy flow to carbon fixation in the form of ATP and NADPH. We isolated a new type of PBS without an allophycocyanin core (i.e., CpcL-PBS). CpcL-PBS contains both a spectral red-shifted chromophore, enabling efficient energy transfer to chlorophyll molecules in the reaction centers, and an increased FNR L content with various rod lengths. Identification of a close association of FNR L with both CpcG-PBS and CpcL-PBS brings new insight to its regulatory role for fine-tuning light energy transfer and carbon fixation through both noncyclic and cyclic electron transport.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ORCiD logo; ; ORCiD logo;
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1508182
Grant/Contract Number:  
SC0001035; FG02-99ER20350
Resource Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online) Journal Volume: 10 Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English

Citation Formats

Liu, Haijun, Weisz, Daniel A., Zhang, Mengru M., Cheng, Ming, Zhang, Bojie, Zhang, Hao, Gerstenecker, Gary S., Pakrasi, Himadri B., Gross, Michael L., Blankenship, Robert E., and McFall-Ngai, ed., Margaret J. Phycobilisomes Harbor FNR L in Cyanobacteria. United States: N. p., 2019. Web. doi:10.1128/mBio.00669-19.
Liu, Haijun, Weisz, Daniel A., Zhang, Mengru M., Cheng, Ming, Zhang, Bojie, Zhang, Hao, Gerstenecker, Gary S., Pakrasi, Himadri B., Gross, Michael L., Blankenship, Robert E., & McFall-Ngai, ed., Margaret J. Phycobilisomes Harbor FNR L in Cyanobacteria. United States. doi:10.1128/mBio.00669-19.
Liu, Haijun, Weisz, Daniel A., Zhang, Mengru M., Cheng, Ming, Zhang, Bojie, Zhang, Hao, Gerstenecker, Gary S., Pakrasi, Himadri B., Gross, Michael L., Blankenship, Robert E., and McFall-Ngai, ed., Margaret J. Tue . "Phycobilisomes Harbor FNR L in Cyanobacteria". United States. doi:10.1128/mBio.00669-19.
@article{osti_1508182,
title = {Phycobilisomes Harbor FNR L in Cyanobacteria},
author = {Liu, Haijun and Weisz, Daniel A. and Zhang, Mengru M. and Cheng, Ming and Zhang, Bojie and Zhang, Hao and Gerstenecker, Gary S. and Pakrasi, Himadri B. and Gross, Michael L. and Blankenship, Robert E. and McFall-Ngai, ed., Margaret J.},
abstractNote = {ABSTRACT Cyanobacterial phycobilisomes (PBSs) are photosynthetic antenna complexes that harvest light energy and supply it to two reaction centers (RCs) where photochemistry starts. PBSs can be classified into two types, depending on the presence of allophycocyanin (APC): CpcG-PBS and CpcL-PBS. Because the accurate protein composition of CpcL-PBS remains unclear, we describe here its isolation and characterization from the cyanobacterium Synechocystis sp. strain 6803. We found that ferredoxin-NADP + oxidoreductase (or FNR L ), an enzyme involved in both cyclic electron transport and the terminal step of the electron transport chain in oxygenic photosynthesis, is tightly associated with CpcL-PBS as well as with CpcG-PBS. Room temperature and low-temperature fluorescence analyses show a red-shifted emission at 669 nm in CpcL-PBS as a terminal energy emitter without APC. SDS-PAGE and quantitative mass spectrometry reveal an increased content of FNR L and CpcC2, a rod linker protein, in CpcL-PBS compared to that of CpcG-PBS rods, indicative of an elongated CpcL-PBS rod length and its potential functional differences from CpcG-PBS. Furthermore, we combined isotope-encoded cross-linking mass spectrometry with computational protein structure predictions and structural modeling to produce an FNR L -PBS binding model that is supported by two cross-links between K 69 of FNR L and the N terminus of CpcB, one component in PBS, in both CpcG-PBS and CpcL-PBS (cross-link 1), and between the N termini of FNR L and CpcB (cross-link 2). Our data provide a novel functional assembly form of phycobiliproteins and a molecular-level description of the close association of FNR L with phycocyanin in both CpcG-PBS and CpcL-PBS. IMPORTANCE Cyanobacterial light-harvesting complex PBSs are essential for photochemistry in light reactions and for balancing energy flow to carbon fixation in the form of ATP and NADPH. We isolated a new type of PBS without an allophycocyanin core (i.e., CpcL-PBS). CpcL-PBS contains both a spectral red-shifted chromophore, enabling efficient energy transfer to chlorophyll molecules in the reaction centers, and an increased FNR L content with various rod lengths. Identification of a close association of FNR L with both CpcG-PBS and CpcL-PBS brings new insight to its regulatory role for fine-tuning light energy transfer and carbon fixation through both noncyclic and cyclic electron transport.},
doi = {10.1128/mBio.00669-19},
journal = {mBio (Online)},
number = 2,
volume = 10,
place = {United States},
year = {2019},
month = {4}
}

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DOI: 10.1128/mBio.00669-19

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