Evolutionary pathways of repeat protein topology in bacterial outer membrane proteins
Abstract
Outer membrane proteins (OMPs) are the proteins in the surface of Gram-negative bacteria. These proteins have diverse functions but a single topology: the β-barrel. Sequence analysis has suggested that this common fold is a β-hairpin repeat protein, and that amplification of the β-hairpin has resulted in 8-26-stranded barrels. Using an integrated approach that combines sequence and structural analyses we find events in which non-amplification diversification also increases barrel strand number. Our network-based analysis reveals strand-number evolutionary pathways, including one that progresses from a primordial 8-stranded barrel to 16-strands and further, to 18-strands. Among these are mechanisms of strand number accretion without domain duplication, like a loop-to-hairpin transition. These mechanisms illustrate perpetuation of repeat protein topology without genetic duplication, likely induced by the hydrophobic membrane. Finally, we find that the evolutionary trace is particularly prominent in the C-terminal half of OMPs, implicating this region in the nucleation of OMP folding.
Data availability
All data generated is available on the website http:// cytostruct.info /rachel/protos/index.html. Summary files of the results are included in the supplement. Software is available on github https://github.com/SluskyLab/PolarBearal.git as are the a3m files https://github.com/SluskyLab/OMBB_A3Mfiles.git
Article and author information
Author details
Funding
National Institute of General Medical Sciences (DP2GM128201)
- Meghan Whitney Franklin
- Joanna SG Slusky
Gordon and Betty Moore Foundation (Moore Inventor Fellowship)
- Joanna SG Slusky
National Science Foundation (MCB160205)
- Joanna SG Slusky
Israel Science Foundation (450/16)
- Nir Ben-Tal
- Rachel Kolodny
National Institute of General Medical Sciences (P20GM103418)
- Meghan Whitney Franklin
- Joanna SG Slusky
National Institute of General Medical Sciences (P20GM113117)
- Meghan Whitney Franklin
- Joanna SG Slusky
National Institute of General Medical Sciences (T32-GM008359)
- Meghan Whitney Franklin
- Joanna SG Slusky
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Vikas Nanda, Rutgers University, United States
Version history
- Received: July 20, 2018
- Accepted: November 28, 2018
- Accepted Manuscript published: November 29, 2018 (version 1)
- Version of Record published: January 21, 2019 (version 2)
Copyright
© 2018, Franklin et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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