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Title: Energetic cost of protein import across the envelope membranes of chloroplasts

Abstract

Chloroplasts are the organelles of green plants in which light energy is transduced into chemical energy, forming ATP and reduced carbon compounds upon which all life depends. The expenditure of this energy is one of the central issues of cellular metabolism. Chloroplasts contain ~3,000 proteins, among which less than 100 are typically encoded in the plastid genome. The rest are encoded in the nuclear genome, synthesized in the cytosol, and posttranslationally imported into the organelle in an energy-dependent process. We report here a measurement of the amount of ATP hydrolyzed to import a protein across the chloroplast envelope membranes--only the second complete accounting of the cost in Gibbs free energy of protein transport to be undertaken. Using two different precursors prepared by three distinct techniques, we show that the import of a precursor protein into chloroplasts is accompanied by the hydrolysis of ~650 ATP molecules. This translates to a ΔGprotein transport of some 27,300 kJ/mol protein imported. Here, we estimate that protein import across the plastid envelope membranes consumes ~0.6% of the total light-saturated energy output of the organelle.

Authors:
 [1];  [1]
  1. Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Davis, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1490431
Grant/Contract Number:  
FG02-03ER15405
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 110; Journal Issue: 3; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; translocation ATPase; chloroplast translocons at inner and outer envelop membranes; import machineries; protein trafficking; cellular energy budget

Citation Formats

Shi, Lan -Xin, and Theg, Steven M. Energetic cost of protein import across the envelope membranes of chloroplasts. United States: N. p., 2013. Web. doi:10.1073/pnas.1115886110.
Shi, Lan -Xin, & Theg, Steven M. Energetic cost of protein import across the envelope membranes of chloroplasts. United States. doi:10.1073/pnas.1115886110.
Shi, Lan -Xin, and Theg, Steven M. Tue . "Energetic cost of protein import across the envelope membranes of chloroplasts". United States. doi:10.1073/pnas.1115886110. https://www.osti.gov/servlets/purl/1490431.
@article{osti_1490431,
title = {Energetic cost of protein import across the envelope membranes of chloroplasts},
author = {Shi, Lan -Xin and Theg, Steven M.},
abstractNote = {Chloroplasts are the organelles of green plants in which light energy is transduced into chemical energy, forming ATP and reduced carbon compounds upon which all life depends. The expenditure of this energy is one of the central issues of cellular metabolism. Chloroplasts contain ~3,000 proteins, among which less than 100 are typically encoded in the plastid genome. The rest are encoded in the nuclear genome, synthesized in the cytosol, and posttranslationally imported into the organelle in an energy-dependent process. We report here a measurement of the amount of ATP hydrolyzed to import a protein across the chloroplast envelope membranes--only the second complete accounting of the cost in Gibbs free energy of protein transport to be undertaken. Using two different precursors prepared by three distinct techniques, we show that the import of a precursor protein into chloroplasts is accompanied by the hydrolysis of ~650 ATP molecules. This translates to a ΔGprotein transport of some 27,300 kJ/mol protein imported. Here, we estimate that protein import across the plastid envelope membranes consumes ~0.6% of the total light-saturated energy output of the organelle.},
doi = {10.1073/pnas.1115886110},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 3,
volume = 110,
place = {United States},
year = {2013},
month = {1}
}

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Free Publicly Available Full Text
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Cited by: 23 works
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Figures / Tables:

Fig. 1 Fig. 1: Inhibition by tentoxin of background ATPase activity in chloroplasts. Chloroplasts were incubated at room temperature in the dark for 10 min in IB containing tentoxin as indicated. ATP mixed with [γ-32P]-ATP was then added to final concentration of 1 mM. Samples were withdrawn at 0 and 30 minmore » after adding ATP. Reactions were stopped by adding an ice-cold acidic charcoal solution. After separating Pi from ATP and other nucleotides using charcoal (Materials and Methods), released [32P] was quantified by scintillation counting. Each point on the graph is the mean of at least three replicates; error bars represent SD.« less

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