Effects of the protonophore carbonyl-cyanide m-chlorophenylhydrazone on intracytoplasmic membrane assembly in Rhodobacter sphaeroides

Woronowicz, Kamil; Olubanjo, Oluwatobi B.; Sha, Daniel; Kay, Joseph M.; Niederman, Robert A.

doi:10.1016/j.bbabio.2015.06.002

Title: Effects of the protonophore carbonyl-cyanide m-chlorophenylhydrazone on intracytoplasmic membrane assembly in Rhodobacter sphaeroides

Journal Article · Thu Oct 01 00:00:00 EDT 2015 · Biochimica et Biophysica Acta - Bioenergetics

DOI:https://doi.org/10.1016/j.bbabio.2015.06.002· OSTI ID:1328132

Woronowicz, Kamil; Olubanjo, Oluwatobi B.; Sha, Daniel; Kay, Joseph M.; Niederman, Robert A.

The effect of carbonyl-cyanide m-chlorophenyl-hydrazone (CCCP) on intracytoplasmic membrane (ICM) assembly was examined in the purple bacterium Rhodobacter sphaeroides. CCCP blocks generation of the electrochemical proton gradient required for integral membrane protein insertion. ICM formation was induced for 8 h, followed by a 4-h exposure to CCCP. Measurements of fluorescence induction/relaxation kinetics showed that CCCP caused a diminished quantum yield, a cessation in expansion of the functional absorption cross-section and a 4- to 10-fold slowing in the electron transfer turnover rate. ICM vesicles (chromatophores) and an upper-pigmented band (UPB) containing ICM growth initiation sites, were isolated and subjected to clear-native electrophoresis. Proteomic analysis of the chromatophore gel bands indicated that CCCP produced a 2.7-fold reduction in spectral counts in the preferentially assembled light-harvesting 2 (LH2) antenna, while the RC-LH1 complex, F₁F_O-ATPase and pyridine nucleotide transhydrogenase decreased by 1.7–1.9-fold. For 35 soluble enzymes, the ratio of 0.99 for treated/control proteins demonstrated that protein synthesis was unaffected by CCCP, suggesting that the membrane complex decline arose from the turnover of unassembled apoproteins. In conclusion, in the UPB fraction, an ~ 2-fold accumulation was observed for the preprotein translocase SecY, the SecA translocation ATPase, SecD and SecF insertion components, and chaperonins DnaJ and DnaK, consistent with the possibility that these factors, which act early in the assembly process, have accumulated in association with nascent polypeptides as stabilized assembly intermediates

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Research Organization:: Rutgers Univ., Piscataway, NJ (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)

Grant/Contract Number:: FG02-08ER15957

OSTI ID:: 1328132

Alternate ID(s):: OSTI ID: 1434925

Journal Information:: Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1847 Journal Issue: 10; ISSN 0005-2728

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 6 works

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References (52)

Crystal structure of a bacterial signal peptidase in complex with a β-lactam inhibitor Paetzel, Mark; Dalbey, Ross E.; Strynadka, Natalie C. J. Nature, Vol. 396, Issue 6707 https://doi.org/10.1038/24196	journal	November 1998
Formation of the b Subunit Dimer Is Necessary for Interaction with F₁-ATPase Sorgen, Paul L.; Bubb, Michael R.; McCormick, Kimberly A. Biochemistry, Vol. 37, Issue 3 https://doi.org/10.1021/bi972309+	journal	January 1998
Differential assembly of polypeptides of the light-harvesting 2 complex encoded by distinct operons during acclimation of Rhodobacter sphaeroides to low light intensity Woronowicz, Kamil; Olubanjo, Oluwatobi B.; Sung, Hee Chang Photosynthesis Research, Vol. 108, Issue 2-3 https://doi.org/10.1007/s11120-011-9681-x	journal	August 2011
Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides Cartron, Michaël L.; Olsen, John D.; Sener, Melih Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10 https://doi.org/10.1016/j.bbabio.2014.02.003	journal	October 2014
Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG–SecDF–YajC–YidC Schulze, Ryan J.; Komar, Joanna; Botte, Mathieu Proceedings of the National Academy of Sciences, Vol. 111, Issue 13 https://doi.org/10.1073/pnas.1315901111	journal	February 2014
Action of the Chaperonin GroEL/ES on a Non-native Substrate Observed with Single-Molecule FRET Kim, So Yeon; Miller, Erik J.; Frydman, Judith Journal of Molecular Biology, Vol. 401, Issue 4 https://doi.org/10.1016/j.jmb.2010.06.050	journal	August 2010
The Accumulation of the Light-Harvesting 2 Complex during Remodeling of the Rhodobacter sphaeroides Intracytoplasmic Membrane Results in a Slowing of the Electron Transfer Turnover Rate of Photochemical Reaction Centers Woronowicz, Kamil; Sha, Daniel; Frese, Raoul N. Biochemistry, Vol. 50, Issue 22 https://doi.org/10.1021/bi101667e	journal	June 2011
Quantitative proteomic analysis of intracytoplasmic membrane development in Rhodobacter sphaeroides: Proteomics of membrane assembly in Rba. sphaeroides Jackson, Philip J.; Lewis, Hilary J.; Tucker, Jaimey D. Molecular Microbiology, Vol. 84, Issue 6 https://doi.org/10.1111/j.1365-2958.2012.08074.x	journal	May 2012
Effect of uncoupler on assembly pathway for pigment-binding protein of bacterial photosynthetic membranes. Dierstein, R.; Drews, G. Journal of Bacteriology, Vol. 168, Issue 1 https://doi.org/10.1128/JB.168.1.167-172.1986	journal	January 1986
Accumulation of the D2 Protein Is a Key Regulatory Step for Assembly of the Photosystem II Reaction Center Complex in Synechocystis PCC 6803 Komenda, Josef; Reisinger, Veronika; Müller, Bernd Christian Journal of Biological Chemistry, Vol. 279, Issue 47 https://doi.org/10.1074/jbc.M405725200	journal	September 2004
High Resolution Clear Native Electrophoresis for In-gel Functional Assays and Fluorescence Studies of Membrane Protein Complexes Wittig, Ilka; Karas, Michael; Schägger, Hermann Molecular & Cellular Proteomics, Vol. 6, Issue 7 https://doi.org/10.1074/mcp.M700076-MCP200	journal	April 2007
Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles: Membrane biogenesis in Rba. sphaeroides Tucker, Jaimey D.; Siebert, C. Alistair; Escalante, Maryana Molecular Microbiology, Vol. 76, Issue 4 https://doi.org/10.1111/j.1365-2958.2010.07153.x	journal	April 2010
Mass Spectrometry-based Protein Profiling to Determine the Cause of Lysosomal Storage Diseases of Unknown Etiology* Sleat, David E.; Ding, Lin; Wang, Shudan Molecular & Cellular Proteomics, Vol. 8, Issue 7 https://doi.org/10.1074/mcp.M900122-MCP200	journal	July 2009
Cellular Functions, Mechanism of Action, and Regulation of ftsh Protease Ito, Koreaki; Akiyama, Yoshinori Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121316	journal	October 2005
The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins Tavernarakis, Nektarios; Driscoll, Monica; Kyrpides, Nikos C. Trends in Biochemical Sciences, Vol. 24, Issue 11 https://doi.org/10.1016/S0968-0004(99)01467-X	journal	November 1999
The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides Hunter, C. Neil; Tucker, Jamey D.; Niederman, Robert A. Photochemical & Photobiological Sciences, Vol. 4, Issue 12 https://doi.org/10.1039/b506099k	journal	January 2005
The Intracytoplasmic Membranes of Purple Bacteria - Assembly of Energy-Transducing Complexes Drews, Gerhart Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 1-2 https://doi.org/10.1159/000346518	journal	January 2013
A conserved function of YidC in the biogenesis of respiratory chain complexes van der Laan, M.; Urbanus, M. L.; ten Hagen-Jongman, C. M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 10 https://doi.org/10.1073/pnas.0636761100	journal	April 2003
Membrane biogenesis in anoxygenic photosynthetic prokaryotes Drews, Gerhart; Niederman, Robert A. Photosynthesis Research, Vol. 73, Issue 1/3, p. 87-94 https://doi.org/10.1023/A:1020481132492	journal	January 2002
Detection of cross-links between FtsH, YidC, HflK/C suggests a linked role for these proteins in quality control upon insertion of bacterial inner membrane proteins van Bloois, Edwin; Dekker, Henk L.; Fröderberg, Linda FEBS Letters, Vol. 582, Issue 10 https://doi.org/10.1016/j.febslet.2008.02.082	journal	April 2008
Tyrosine phosphorylation in Escherichia coli Freestone, Primrose; Trinei, Mirella; Clarke, Stuart C. Journal of Molecular Biology, Vol. 279, Issue 5 https://doi.org/10.1006/jmbi.1998.1836	journal	June 1998
Oligomeric Characterization of the Photosynthetic Apparatus of Rhodobacter sphaeroides R26.1 by Nondenaturing Electrophoresis Methods D’Amici, Gian Maria; Rinalducci, Sara; Murgiano, Leonardo Journal of Proteome Research, Vol. 9, Issue 1 https://doi.org/10.1021/pr9005052	journal	January 2010
YidC Occupies the Lateral Gate of the SecYEG Translocon and Is Sequentially Displaced by a Nascent Membrane Protein Sachelaru, Ilie; Petriman, Narcis Adrian; Kudva, Renuka Journal of Biological Chemistry, Vol. 288, Issue 23 https://doi.org/10.1074/jbc.M112.446583	journal	April 2013
Formation of the light-harvesting complex I (B870) of anoxygenic phototrophic purple bacteria Drews, G. Archives of Microbiology, Vol. 166, Issue 3 https://doi.org/10.1007/s002030050370	journal	September 1996
Uncoupling of Oxidative Phosphorylation by Carbonyl Cyanide Phenylhydrazones. I. Some Characteristics of m-CI-CCP Action on Mitochondria and Chloroplasts Heytler, P. G. Biochemistry, Vol. 2, Issue 2 https://doi.org/10.1021/bi00902a031	journal	March 1963
Structural and Functional Proteomics of Intracytoplasmic Membrane Assembly in <b><i>Rhodobacter sphaeroides</i></b> Woronowicz, Kamil; Harrold, John W.; Kay, Joseph M. Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 1-2 https://doi.org/10.1159/000346520	journal	January 2013
Three-dimensional structure of the bacterial protein-translocation complex SecYEG Breyton, Cécile; Haase, Winfried; Rapoport, Tom A. Nature, Vol. 418, Issue 6898 https://doi.org/10.1038/nature00827	journal	August 2002
Mechanism of action of agents which uncouple oxidative phosphorylation: Direct correlation between protoncarrying and respiratory-releasing properties using rat liver mitochondria Cunarro, Julia; Weiner, Michael W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 387, Issue 2 https://doi.org/10.1016/0005-2728(75)90106-1	journal	May 1975
Oligomerization states and associations of light-harvesting pigment-protein complexes of Rhodobacter sphaeroides as analyzed by lithium dodecyl sulfate-polyacrylamide gel electrophoresis Hunter, C. Neil; Pennoyer, Jeffrey D.; Sturgis, James N. Biochemistry, Vol. 27, Issue 9 https://doi.org/10.1021/bi00409a050	journal	May 1988
SecDFyajC forms a heterotetrameric complex with YidC: SecDFyajC-YidC complex formation Nouwen, Nico; Driessen, Arnold J. M. Molecular Microbiology, Vol. 44, Issue 5 https://doi.org/10.1046/j.1365-2958.2002.02972.x	journal	May 2002
The Psb27 Assembly Factor Binds to the CP43 Complex of Photosystem II in the Cyanobacterium Synechocystis sp. PCC 6803 Komenda, Josef; Knoppová, Jana; Kopečná, Jana Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/pp.111.184184	journal	November 2011
Rhodobacter capsulatus CycH: a bipartite gene product with pleiotropic effects on the biogenesis of structurally different c-type cytochromes. Lang, S. E.; Jenney, F. E.; Daldal, F. Journal of bacteriology, Vol. 178, Issue 17 https://doi.org/10.1128/JB.178.17.5279-5290.1996	journal	January 1996
Assembly of Multimeric Proteins Ahmad, Suhail; Glavas, Natalie A.; Bragg, Philip D. Journal of Molecular Biology, Vol. 234, Issue 1 https://doi.org/10.1006/jmbi.1993.1559	journal	November 1993
The native architecture of a photosynthetic membrane Bahatyrova, Svetlana; Frese, Raoul N.; Siebert, C. Alistair Nature, Vol. 430, Issue 7003 https://doi.org/10.1038/nature02823	journal	August 2004
Import and assembly of the ? and ?-polypeptides of the light-harvesting complex I (B870) in the membrane system of Rhodobacter capsulatus investigated in an in vitro translation system Meryandini, Anja; Drews, Gerhart Photosynthesis Research, Vol. 47, Issue 1 https://doi.org/10.1007/BF00017750	journal	January 1996
SPECTRA AND EXTINCTION COEFFICIENTS OF NEAR-INFRARED ABSORPTION BANDS IN MEMBRANES OF Rhodobacter sphaeroides MUTANTS LACKING LIGHT-HARVESTING AND REACTION CENTER COMPLEXES Sturgis, James N.; Hunter, C. Neil; Niederman, Robert A. Photochemistry and Photobiology, Vol. 48, Issue 2 https://doi.org/10.1111/j.1751-1097.1988.tb02817.x	journal	August 1988
Eukaryotic behaviour of a prokaryotic energy-transducing membrane: fully detached vesicular organelles arise by budding from the Rhodobacter sphaeroides intracytoplasmic photosynthetic membrane: Intracytoplasmic membrane budding in a photosynthetic prokaryote Niederman, Robert A. Molecular Microbiology, Vol. 76, Issue 4 https://doi.org/10.1111/j.1365-2958.2010.07154.x	journal	April 2010
The Rieske protein from Paracoccus denitrificans is inserted into the cytoplasmic membrane by the twin-arginine translocase Bachmann, Julie; Bauer, Brigitte; Zwicker, Klaus FEBS Journal, Vol. 273, Issue 21 https://doi.org/10.1111/j.1742-4658.2006.05480.x	journal	November 2006
Sequential assembly of photosynthetic units in Rhodobacter sphaeroides as revealed by fast repetition rate analysis of variable bacteriochlorophyll a fluorescence Koblízek, Michal; Shih, Joseph D.; Breitbart, Seth I. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 3 https://doi.org/10.1016/j.bbabio.2004.11.004	journal	February 2005
YidC Protein, a Molecular Chaperone for LacY Protein Folding via the SecYEG Protein Machinery Zhu, Lu; Kaback, H. Ronald; Dalbey, Ross E. Journal of Biological Chemistry, Vol. 288, Issue 39 https://doi.org/10.1074/jbc.M113.491613	journal	August 2013
YidC Is Strictly Required for Membrane Insertion of Subunits a and c of the F ₁ F ₀ ATP Synthase and SecE of the SecYEG Translocase ^† Yi, Liang; Jiang, Fenglei; Chen, Minyong Biochemistry, Vol. 42, Issue 35 https://doi.org/10.1021/bi034309h	journal	September 2003
Fast oxidation of the primary electron acceptor under anaerobic conditions requires the organization of the photosynthetic chain of Rhodobacter sphaeroides in supercomplexes Joliot, Pierre; Joliot, Anne; Verméglio, André Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 3 https://doi.org/10.1016/j.bbabio.2004.11.002	journal	February 2005
Differential Roles of the Universal Stress Proteins of Escherichia coli in Oxidative Stress Resistance, Adhesion, and Motility Nachin, L.; Nannmark, U.; Nystrom, T. Journal of Bacteriology, Vol. 187, Issue 18 https://doi.org/10.1128/JB.187.18.6265-6272.2005	journal	September 2005
A Genomic Perspective on Protein Families Tatusov, R. L. Science, Vol. 278, Issue 5338 https://doi.org/10.1126/science.278.5338.631	journal	October 1997
Psb28 Protein Is Involved in the Biogenesis of the Photosystem II Inner Antenna CP47 (PsbB) in the Cyanobacterium Synechocystis sp. PCC 6803 Dobáková, Marika; Sobotka, Roman; Tichý, Martin Plant Physiology, Vol. 149, Issue 2 https://doi.org/10.1104/pp.108.130039	journal	November 2008
An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting Papagiannakis, E.; Kennis, J. T. M.; van Stokkum, I. H. M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.092626599	journal	April 2002
YidC mediates membrane protein insertion in bacteria Samuelson, James C.; Chen, Minyong; Jiang, Fenglei Nature, Vol. 406, Issue 6796 https://doi.org/10.1038/35020586	journal	August 2000
Aberrant Assembly Complexes of the Reaction Center Light-harvesting 1 PufX (RC-LH1-PufX) Core Complex of Rhodobacter sphaeroides Imaged by Atomic Force Microscopy Olsen, John D.; Adams, Peter G.; Jackson, Philip J. Journal of Biological Chemistry, Vol. 289, Issue 43 https://doi.org/10.1074/jbc.M114.596585	journal	September 2014
The effects of protein crowding in bacterial photosynthetic membranes on the flow of quinone redox species between the photochemical reaction center and the ubiquinol-cytochrome c2 oxidoreductase Woronowicz, Kamil; Sha, Daniel; Frese, Raoul N. Metallomics, Vol. 3, Issue 8 https://doi.org/10.1039/c1mt00034a	journal	January 2011
Proteomic Characterization of the Rhodobacter sphaeroides 2.4.1 Photosynthetic Membrane: Identification of New Proteins Zeng, Xiaohua; Roh, Jung Hyeob; Callister, Stephen J. Journal of Bacteriology, Vol. 189, Issue 20 https://doi.org/10.1128/JB.00946-07	journal	August 2007
Membrane development in purple photosynthetic bacteria in response to alterations in light intensity and oxygen tension Niederman, Robert A. Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9851-0	journal	May 2013
Assembly of photosynthetic apparatus in Rhodobacter sphaeroides as revealed by functional assessments at different growth phases and in synchronized and greening cells Kis, M.; Asztalos, E.; Sipka, G. Photosynthesis Research, Vol. 122, Issue 3 https://doi.org/10.1007/s11120-014-0026-4	journal	July 2014

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59 BASIC BIOLOGICAL SCIENCES
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reaction center
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Title: Effects of the protonophore carbonyl-cyanide m-chlorophenylhydrazone on intracytoplasmic membrane assembly in Rhodobacter sphaeroides

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