Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported

Shatsky, Maxim; Allen, Simon; Gold, Barbara L.; Liu, Nancy L.; Juba, Thomas R.; Reveco, Sonia A.; Elias, Dwayne A.; Prathapam, Ramadevi; He, Jennifer; Yang, Wenhong; Szakal, Evelin D.; Liu, Haichuan; Singer, Mary E.; Geller, Jil T.; Lam, Bonita R.; Saini, Avneesh; Trotter, Valentine V.; Hall, Steven C.; Fisher, Susan J.; Brenner, Steven E.; Chhabra, Swapnil R.; Hazen, Terry C.; Wall, Judy D.; Witkowska, H. Ewa; Biggin, Mark D.; Chandonia, John-Marc; Butland, Gareth

doi:10.1074/mcp.M115.054692

Title: Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported

Journal Article · Sun May 01 00:00:00 EDT 2016 · Molecular and Cellular Proteomics

DOI:https://doi.org/10.1074/mcp.M115.054692· OSTI ID:1766619

Shatsky, Maxim; Allen, Simon; Gold, Barbara L.; Liu, Nancy L.; Juba, Thomas R.; Reveco, Sonia A.; Elias, Dwayne A.; Prathapam, Ramadevi; He, Jennifer; Yang, Wenhong; Szakal, Evelin D.; Liu, Haichuan; Singer, Mary E.; Geller, Jil T.; Lam, Bonita R.; Saini, Avneesh; Trotter, Valentine V.; Hall, Steven C.; Fisher, Susan J.; Brenner, Steven E. more »

© 2016 by The American Society for Biochemistry and Molecular Biology, Inc. Numerous affinity purification-mass spectrometry (APMS) and yeast two-hybrid screens have each defined thousands of pairwise protein-protein interactions (PPIs), most of which are between functionally unrelated proteins. The accuracy of these networks, however, is under debate. Here, we present an AP-MS survey of the bacterium Desulfovibrio vulgaris together with a critical reanalysis of nine published bacterial yeast two-hybrid and AP-MS screens. We have identified 459 high confidence PPIs from D. vulgaris and 391 from Escherichia coli. Compared with the nine published interactomes, our two networks are smaller, are much less highly connected, and have significantly lower false discovery rates. In addition, our interactomes are much more enriched in protein pairs that are encoded in the same operon, have similar functions, and are reproducibly detected in other physical interaction assays than the pairs reported in prior studies. Our work establishes more stringent benchmarks for the properties of protein interactomes and suggests that bona fide PPIs much more frequently involve protein partners that are annotated with similar functions or that can be validated in independent assays than earlier studies suggested.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02–05CH11231; AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1766619

Alternate ID(s):: OSTI ID: 1261350; OSTI ID: 1379316

Journal Information:: Molecular and Cellular Proteomics, Journal Name: Molecular and Cellular Proteomics Vol. 15 Journal Issue: 5; ISSN 1535-9476

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 10 works

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References (57)

An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: Exploration by an integrative approach Marchadier, Elodie; Carballido-López, Rut; Brinster, Sophie PROTEOMICS, Vol. 11, Issue 15 https://doi.org/10.1002/pmic.201000791	journal	May 2011
Proteome survey reveals modularity of the yeast cell machinery Gavin, Anne-Claude; Aloy, Patrick; Grandi, Paola Nature, Vol. 440, Issue 7084 https://doi.org/10.1038/nature04532	journal	January 2006
MicrobesOnline: an integrated portal for comparative and functional genomics Dehal, P. S.; Joachimiak, M. P.; Price, M. N. Nucleic Acids Research, Vol. 38, Issue suppl_1, p. D396-D400 https://doi.org/10.1093/nar/gkp919	journal	November 2009
The Binary Protein Interactome of Treponema pallidum – The Syphilis Spirochete Titz, Björn; Rajagopala, Seesandra V.; Goll, Johannes PLoS ONE, Vol. 3, Issue 5 https://doi.org/10.1371/journal.pone.0002292	journal	May 2008
Correlation of two-hybrid affinity data with in vitro measurements. Estojak, J.; Brent, R.; Golemis, E. A. Molecular and Cellular Biology, Vol. 15, Issue 10 https://doi.org/10.1128/MCB.15.10.5820	journal	October 1995
SnapShot: Protein-Protein Interaction Networks Seebacher, Jan; Gavin, Anne-Claude Cell, Vol. 144, Issue 6 https://doi.org/10.1016/j.cell.2011.02.025	journal	March 2011
The comprehensive microbial resource Davidsen, Tanja; Beck, Erin; Ganapathy, Anuradha Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp912	journal	November 2009
High-Quality Binary Protein Interaction Map of the Yeast Interactome Network Yu, H.; Braun, P.; Yildirim, M. A. Science, Vol. 322, Issue 5898 https://doi.org/10.1126/science.1158684	journal	October 2008
A Second-generation Protein–Protein Interaction Network of Helicobacter pylori Häuser, Roman; Ceol, Arnaud; Rajagopala, Seesandra V. Molecular & Cellular Proteomics, Vol. 13, Issue 5 https://doi.org/10.1074/mcp.O113.033571	journal	March 2014
Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Elias, Joshua E.; Gygi, Steven P. Nature Methods, Vol. 4, Issue 3 https://doi.org/10.1038/nmeth1019	journal	February 2007
A Protein Complex Network of Drosophila melanogaster Guruharsha, K. G.; Rual, Jean-François; Zhai, Bo Cell, Vol. 147, Issue 3 https://doi.org/10.1016/j.cell.2011.08.047	journal	October 2011
Survey of large protein complexes in D. vulgaris reveals great structural diversity Han, B. -G.; Dong, M.; Liu, H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 39 https://doi.org/10.1073/pnas.0813068106	journal	September 2009
The MIntAct project—IntAct as a common curation platform for 11 molecular interaction databases Orchard, Sandra; Ammari, Mais; Aranda, Bruno Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1115	journal	November 2013
Panorama: A Targeted Proteomics Knowledge Base Sharma, Vagisha; Eckels, Josh; Taylor, Greg K. Journal of Proteome Research, Vol. 13, Issue 9 https://doi.org/10.1021/pr5006636	journal	July 2014
The binary protein-protein interaction landscape of Escherichia coli Rajagopala, Seesandra V.; Sikorski, Patricia; Kumar, Ashwani Nature Biotechnology, Vol. 32, Issue 3 https://doi.org/10.1038/nbt.2831	journal	February 2014
SAINT: probabilistic scoring of affinity purification–mass spectrometry data Choi, Hyungwon; Larsen, Brett; Lin, Zhen-Yuan Nature Methods, Vol. 8, Issue 1 https://doi.org/10.1038/nmeth.1541	journal	December 2010
Sequential Peptide Affinity (SPA) System for the Identification of Mammalian and Bacterial Protein Complexes Zeghouf, Mahel; Li, Joyce; Butland, Gareth Journal of Proteome Research, Vol. 3, Issue 3 https://doi.org/10.1021/pr034084x	journal	June 2004
Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome Díaz-Mejía, Juan Javier; Babu, Mohan; Emili, Andrew FEMS Microbiology Reviews, Vol. 33, Issue 1 https://doi.org/10.1111/j.1574-6976.2008.00141.x	journal	January 2009
Proteome Organization in a Genome-Reduced Bacterium Kühner, Sebastian; van Noort, Vera; Betts, Matthew J. Science, Vol. 326, Issue 5957 https://doi.org/10.1126/science.1176343	journal	November 2009
Protein–protein interaction networks: the puzzling riches Wodak, Shoshana J.; Vlasblom, James; Turinsky, Andrei L. Current Opinion in Structural Biology, Vol. 23, Issue 6 https://doi.org/10.1016/j.sbi.2013.08.002	journal	December 2013
Skyline: an open source document editor for creating and analyzing targeted proteomics experiments MacLean, Brendan; Tomazela, Daniela M.; Shulman, Nicholas Bioinformatics, Vol. 26, Issue 7 https://doi.org/10.1093/bioinformatics/btq054	journal	February 2010
Interactome Networks and Human Disease Vidal, Marc; Cusick, Michael E.; Barabási, Albert-László Cell, Vol. 144, Issue 6 https://doi.org/10.1016/j.cell.2011.02.016	journal	March 2011
Cell-Wide Responses to Low-Oxygen Exposure in Desulfovibrio vulgaris Hildenborough Mukhopadhyay, A.; Redding, A. M.; Joachimiak, M. P. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/JB.00368-07	journal	June 2007
A Proteome-Scale Map of the Human Interactome Network Rolland, Thomas; Taşan, Murat; Charloteaux, Benoit Cell, Vol. 159, Issue 5 https://doi.org/10.1016/j.cell.2014.10.050	journal	November 2014
An empirical framework for binary interactome mapping Venkatesan, Kavitha; Rual, Jean-François; Vazquez, Alexei Nature Methods, Vol. 6, Issue 1 https://doi.org/10.1038/nmeth.1280	journal	December 2008
An experimentally derived confidence score for binary protein-protein interactions Braun, Pascal; Tasan, Murat; Dreze, Matija Nature Methods, Vol. 6, Issue 1 https://doi.org/10.1038/nmeth.1281	journal	December 2008
A proteome-wide protein interaction map for Campylobacter jejuni Parrish, Jodi R.; Yu, Jingkai; Liu, Guozhen Genome Biology, Vol. 8, Issue 7 https://doi.org/10.1186/gb-2007-8-7-r130	journal	January 2007
Generalized Schemes for High-Throughput Manipulation of the Desulfovibrio vulgaris Genome Chhabra, S. R.; Butland, G.; Elias, D. A. Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.05495-11	journal	September 2011
PSORTb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis Gardy, J. L.; Laird, M. R.; Chen, F. Bioinformatics, Vol. 21, Issue 5 https://doi.org/10.1093/bioinformatics/bti057	journal	October 2004
Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network Simonis, Nicolas; Rual, Jean-François; Carvunis, Anne-Ruxandra Nature Methods, Vol. 6, Issue 1 https://doi.org/10.1038/nmeth.1279	journal	December 2008
Towards a Rigorous Network of Protein-Protein Interactions of the Model Sulfate Reducer Desulfovibrio vulgaris Hildenborough Chhabra, Swapnil R.; Joachimiak, Marcin P.; Petzold, Christopher J. PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0021470	journal	June 2011
Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough Zane, G. M.; Yen, H. -c. B.; Wall, J. D. Applied and Environmental Microbiology, Vol. 76, Issue 16 https://doi.org/10.1128/AEM.00691-10	journal	June 2010
DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila Murali, Thilakam; Pacifico, Svetlana; Yu, Jingkai Nucleic Acids Research, Vol. 39, Issue suppl_1 https://doi.org/10.1093/nar/gkq1092	journal	October 2010
Overexpression of biotin synthase and biotin ligase is required for efficient generation of sulfur-35 labeled biotin in E. coli Delli-Bovi, Teegan A.; Spalding, Maroya D.; Prigge, Sean T. BMC Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1186/1472-6750-10-73	journal	January 2010
Global landscape of protein complexes in the yeast Saccharomyces cerevisiae Krogan, Nevan J.; Cagney, Gerard; Yu, Haiyuan Nature, Vol. 440, Issue 7084 https://doi.org/10.1038/nature04670	journal	March 2006
A Large-scale Protein–protein Interaction Analysis in Synechocystis sp. PCC6803 Sato, Shusei; Shimoda, Yoshikazu; Muraki, Akiko DNA Research, Vol. 14, Issue 5 https://doi.org/10.1093/dnares/dsm021	journal	January 2007
Comparative assessment of large-scale data sets of protein–protein interactions von Mering, Christian; Krause, Roland; Snel, Berend Nature, Vol. 417, Issue 6887 https://doi.org/10.1038/nature750	journal	May 2002
Large-scale identification of protein-protein interaction of Escherichia coli K-12 Arifuzzaman, M. Genome Research, Vol. 16, Issue 5 https://doi.org/10.1101/gr.4527806	journal	May 2006
How sulphate-reducing microorganisms cope with stress: lessons from systems biology Zhou, Jizhong; He, Qiang; Hemme, Christopher L. Nature Reviews Microbiology, Vol. 9, Issue 6 https://doi.org/10.1038/nrmicro2575	journal	May 2011
Impact of elevated nitrate on sulfate-reducing bacteria: a comparative Study of Desulfovibrio vulgaris He, Qiang; He, Zhili; Joyner, Dominique C. The ISME Journal, Vol. 4, Issue 11 https://doi.org/10.1038/ismej.2010.59	journal	May 2010
A Global Protein Kinase and Phosphatase Interaction Network in Yeast Breitkreutz, A.; Choi, H.; Sharom, J. R. Science, Vol. 328, Issue 5981 https://doi.org/10.1126/science.1176495	journal	May 2010
High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition Chiu, Y. -L.; Witkowska, H. E.; Hall, S. C. Proceedings of the National Academy of Sciences, Vol. 103, Issue 42 https://doi.org/10.1073/pnas.0604524103	journal	October 2006
Interaction of Fibronectin With Semen Amyloids Synergistically Enhances HIV Infection Roan, Nadia R.; Chu, Simon; Liu, Haichuan The Journal of Infectious Diseases, Vol. 210, Issue 7 https://doi.org/10.1093/infdis/jiu220	journal	April 2014
Flaws in evaluation schemes for pair-input computational predictions Park, Yungki; Marcotte, Edward M. Nature Methods, Vol. 9, Issue 12 https://doi.org/10.1038/nmeth.2259	journal	December 2012
Toward a Comprehensive Atlas of the Physical Interactome of Saccharomyces cerevisiae Collins, Sean R.; Kemmeren, Patrick; Zhao, Xue-Chu Molecular & Cellular Proteomics, Vol. 6, Issue 3 https://doi.org/10.1074/mcp.M600381-MCP200	journal	January 2007
High-throughput Isolation and Characterization of Untagged Membrane Protein Complexes: Outer Membrane Complexes of Desulfovibrio vulgaris Walian, Peter J.; Allen, Simon; Shatsky, Maxim Journal of Proteome Research, Vol. 11, Issue 12 https://doi.org/10.1021/pr300548d	journal	October 2012
Statistical Analysis of Membrane Proteome Expression Changes in Saccharomyces c erevisiae Zybailov, Boris; Mosley, Amber L.; Sardiu, Mihaela E. Journal of Proteome Research, Vol. 5, Issue 9 https://doi.org/10.1021/pr060161n	journal	September 2006
A Model for Random Sampling and Estimation of Relative Protein Abundance in Shotgun Proteomics Liu, Hongbin; Sadygov, Rovshan G.; Yates, John R. Analytical Chemistry, Vol. 76, Issue 14 https://doi.org/10.1021/ac0498563	journal	July 2004
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Analysis of the Human Endogenous Coregulator Complexome Malovannaya, Anna; Lanz, Rainer B.; Jung, Sung Yun Cell, Vol. 145, Issue 5 https://doi.org/10.1016/j.cell.2011.05.006	journal	May 2011
Interaction network containing conserved and essential protein complexes in Escherichia coli Butland, Gareth; Peregrín-Alvarez, José Manuel; Li, Joyce Nature, Vol. 433, Issue 7025 https://doi.org/10.1038/nature03239	journal	February 2005
Global Functional Atlas of Escherichia coli Encompassing Previously Uncharacterized Proteins Hu, Pingzhao; Janga, Sarath Chandra; Babu, Mohan PLoS Biology, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pbio.1000096	journal	April 2009
The Crystal Structure of Desulfovibrio vulgaris Dissimilatory Sulfite Reductase Bound to DsrC Provides Novel Insights into the Mechanism of Sulfate Respiration Oliveira, Tânia F.; Vonrhein, Clemens; Matias, Pedro M. Journal of Biological Chemistry, Vol. 283, Issue 49 https://doi.org/10.1074/jbc.M805643200	journal	September 2008
High throughput strategies for probing the different organizational levels of protein interaction networks Kristensen, Anders R.; Foster, Leonard J. Molecular BioSystems, Vol. 9, Issue 9 https://doi.org/10.1039/c3mb70135b	journal	January 2013
The EcoCyc Database Karp, P. D. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.56	journal	January 2002
Extracting Insight from Noisy Cellular Networks Landry, Christian R.; Levy, Emmanuel D.; Abd Rabbo, Diala Cell, Vol. 155, Issue 5 https://doi.org/10.1016/j.cell.2013.11.003	journal	November 2013
EcoCyc: fusing model organism databases with systems biology Keseler, Ingrid M.; Mackie, Amanda; Peralta-Gil, Martin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1027	journal	November 2012

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