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

Abstract

© 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.

Authors:
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Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
OSTI Identifier:
1766619
Alternate Identifier(s):
OSTI ID: 1261350; OSTI ID: 1379316
Grant/Contract Number:  
AC02–05CH11231; AC05-00OR22725; AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Molecular and Cellular Proteomics
Additional Journal Information:
Journal Name: Molecular and Cellular Proteomics Journal Volume: 15 Journal Issue: 5; Journal ID: ISSN 1535-9476
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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, and Butland, Gareth. Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported. United States: N. p., 2016. Web. doi:10.1074/mcp.M115.054692.
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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. Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported. United States. https://doi.org/10.1074/mcp.M115.054692
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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, and Butland, Gareth. Sun . "Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported". United States. https://doi.org/10.1074/mcp.M115.054692.
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@article{osti_1766619,
title = {Bacterial Interactomes: Interacting Protein Partners Share Similar Function and Are Validated in Independent Assays More Frequently Than Previously Reported},
author = {Shatsky, Maxim and Allen, Simon and Gold, Barbara L. and Liu, Nancy L. and Juba, Thomas R. and Reveco, Sonia A. and Elias, Dwayne A. and Prathapam, Ramadevi and He, Jennifer and Yang, Wenhong and Szakal, Evelin D. and Liu, Haichuan and Singer, Mary E. and Geller, Jil T. and Lam, Bonita R. and Saini, Avneesh and Trotter, Valentine V. and Hall, Steven C. and Fisher, Susan J. and Brenner, Steven E. and Chhabra, Swapnil R. and Hazen, Terry C. and Wall, Judy D. and Witkowska, H. Ewa and Biggin, Mark D. and Chandonia, John-Marc and Butland, Gareth},
abstractNote = {© 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.},
doi = {10.1074/mcp.M115.054692},
journal = {Molecular and Cellular Proteomics},
number = 5,
volume = 15,
place = {United States},
year = {Sun May 01 00:00:00 EDT 2016},
month = {Sun May 01 00:00:00 EDT 2016}
}
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https://doi.org/10.1074/mcp.M115.054692
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