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Title: Structure of the complex I-like molecule NDH of oxygenic photosynthesis

Abstract

Cyclic electron flow around photosystem I (PSI) is a mechanism by which photosynthetic organisms balance the levels of ATP and NADPH necessary for efficient photosynthesis1,2. NAD(P)H dehydrogenase-like complex (NDH) is a key component of this pathway in most oxygenic photosynthetic organisms3,4 and is the last large photosynthetic membrane-protein complex for which the structure remains unknown. Related to the respiratory NADH dehydrogenase complex (complex I), NDH transfers electrons originating from PSI to the plastoquinone pool while pumping protons across the thylakoid membrane, thereby increasing the amount of ATP produced per NADP+ molecule reduced4,5. NDH possesses 11 of the 14 core complex I subunits, as well as several oxygenic-photosynthesis-specific (OPS) subunits that are conserved from cyanobacteria to plants3,6. However, the three core complex I subunits that are involved in accepting electrons from NAD(P)H are notably absent in NDH3,5,6, and it is therefore not clear how NDH acquires and transfers electrons to plastoquinone. It is proposed that the OPS subunits—specifically NdhS—enable NDH to accept electrons from its electron donor, ferredoxin3,4,5,7. Here we report a 3.1 Å structure of the 0.42-MDa NDH complex from the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1, obtained by single-particle cryo-electron microscopy. Our maps reveal the structure and arrangement of themore » principal OPS subunits in the NDH complex, as well as an unexpected cofactor close to the plastoquinone-binding site in the peripheral arm. The location of the OPS subunits supports a role in electron transfer and defines two potential ferredoxin-binding sites at the apex of the peripheral arm. These results suggest that NDH could possess several electron transfer routes, which would serve to maximize plastoquinone reduction and avoid deleterious off-target chemistry of the semi-plastoquinone radical.« less

Authors:
 [1];  [2];  [2];  [3];  [1]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrative Bioimaging Div.
  2. Groupe d'etude des proteines membranaires (GEPROM), Montreal, Quebec (Canada); McGill Univ., Montreal, QC (Canada). Dept. of Pharmacology and Therapeutics
  3. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1501883
DOE Contract Number:  
SC00016240; AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Nature (London)
Additional Journal Information:
Journal Volume: 566; Journal Issue: 7744; Journal ID: ISSN 0028-0836
Country of Publication:
United States
Language:
English

Citation Formats

Laughlin, Thomas G., Bayne, Andrew N., Trempe, Jean-François, Savage, David F., and Davies, Karen M. Structure of the complex I-like molecule NDH of oxygenic photosynthesis. United States: N. p., 2019. Web. doi:10.1038/s41586-019-0921-0.
Laughlin, Thomas G., Bayne, Andrew N., Trempe, Jean-François, Savage, David F., & Davies, Karen M. Structure of the complex I-like molecule NDH of oxygenic photosynthesis. United States. doi:10.1038/s41586-019-0921-0.
Laughlin, Thomas G., Bayne, Andrew N., Trempe, Jean-François, Savage, David F., and Davies, Karen M. Fri . "Structure of the complex I-like molecule NDH of oxygenic photosynthesis". United States. doi:10.1038/s41586-019-0921-0.
@article{osti_1501883,
title = {Structure of the complex I-like molecule NDH of oxygenic photosynthesis},
author = {Laughlin, Thomas G. and Bayne, Andrew N. and Trempe, Jean-François and Savage, David F. and Davies, Karen M.},
abstractNote = {Cyclic electron flow around photosystem I (PSI) is a mechanism by which photosynthetic organisms balance the levels of ATP and NADPH necessary for efficient photosynthesis1,2. NAD(P)H dehydrogenase-like complex (NDH) is a key component of this pathway in most oxygenic photosynthetic organisms3,4 and is the last large photosynthetic membrane-protein complex for which the structure remains unknown. Related to the respiratory NADH dehydrogenase complex (complex I), NDH transfers electrons originating from PSI to the plastoquinone pool while pumping protons across the thylakoid membrane, thereby increasing the amount of ATP produced per NADP+ molecule reduced4,5. NDH possesses 11 of the 14 core complex I subunits, as well as several oxygenic-photosynthesis-specific (OPS) subunits that are conserved from cyanobacteria to plants3,6. However, the three core complex I subunits that are involved in accepting electrons from NAD(P)H are notably absent in NDH3,5,6, and it is therefore not clear how NDH acquires and transfers electrons to plastoquinone. It is proposed that the OPS subunits—specifically NdhS—enable NDH to accept electrons from its electron donor, ferredoxin3,4,5,7. Here we report a 3.1 Å structure of the 0.42-MDa NDH complex from the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1, obtained by single-particle cryo-electron microscopy. Our maps reveal the structure and arrangement of the principal OPS subunits in the NDH complex, as well as an unexpected cofactor close to the plastoquinone-binding site in the peripheral arm. The location of the OPS subunits supports a role in electron transfer and defines two potential ferredoxin-binding sites at the apex of the peripheral arm. These results suggest that NDH could possess several electron transfer routes, which would serve to maximize plastoquinone reduction and avoid deleterious off-target chemistry of the semi-plastoquinone radical.},
doi = {10.1038/s41586-019-0921-0},
journal = {Nature (London)},
issn = {0028-0836},
number = 7744,
volume = 566,
place = {United States},
year = {2019},
month = {2}
}

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