Combining Mutations That Inhibit Two Distinct Steps of the ATP Hydrolysis Cycle Restores Wild-Type Function in the Lipopolysaccharide Transporter and Shows that ATP Binding Triggers Transport
Abstract
ATP-binding cassette (ABC) transporters constitute a large family of proteins present in all domains of life. They are powered by dynamic ATPases that harness energy from binding and hydrolyzing ATP through a cycle that involves the closing and reopening of their two ATP-binding domains. The LptB2FGC exporter is an essential ABC transporter that assembles lipopolysaccharides (LPS) on the surface of Gram-negative bacteria to form a permeability barrier against many antibiotics. LptB2FGC extracts newly synthesized LPS molecules from the inner membrane and powers their transport across the periplasm and through the outer membrane. How LptB2FGC functions remains poorly understood. Here, we show that the C-terminal domain of the dimeric LptB ATPase is essential for LPS transport in Escherichia coli. Specific changes in the C-terminal domain of LptB cause LPS transport defects that can be repaired by intragenic suppressors altering the ATP-binding domains. Surprisingly, we found that each of two lethal changes in the ATP-binding and C-terminal domains of LptB, when present in combined form, suppressed the defects associated with the other to restore LPS transport to wild-type levels both in vivo and in vitro. We present biochemical evidence explaining the effect that each of these mutations has on LptB function andmore »
- Authors:
-
[3]
- The Ohio State Univ., Columbus, OH (United States); Univ. of Georgia, Athens, GA (United States)
- Harvard Univ., Cambridge, MA (United States)
- The Ohio State Univ., Columbus, OH (United States)
- Harvard Univ., Cambridge, MA (United States); Harvard Medical School, Boston, MA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Institutes of Health (NIH)
- OSTI Identifier:
- 1569912
- Grant/Contract Number:
- R01-GM100951; R01-GM066174; R0-AI081059
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 10; Journal Issue: 4; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ABC transporters; ATPase; cell envelope; lipopolysaccharide; outer membrane
Citation Formats
Simpson, Brent W., Pahil, Karanbir S., Owens, Tristan W., Lundstedt, Emily A., Davis, Rebecca M., Kahne, Daniel, and Ruiz, Natividad. Combining Mutations That Inhibit Two Distinct Steps of the ATP Hydrolysis Cycle Restores Wild-Type Function in the Lipopolysaccharide Transporter and Shows that ATP Binding Triggers Transport. United States: N. p., 2019.
Web. doi:10.1128/mbio.01931-19.
Simpson, Brent W., Pahil, Karanbir S., Owens, Tristan W., Lundstedt, Emily A., Davis, Rebecca M., Kahne, Daniel, & Ruiz, Natividad. Combining Mutations That Inhibit Two Distinct Steps of the ATP Hydrolysis Cycle Restores Wild-Type Function in the Lipopolysaccharide Transporter and Shows that ATP Binding Triggers Transport. United States. https://doi.org/10.1128/mbio.01931-19
Simpson, Brent W., Pahil, Karanbir S., Owens, Tristan W., Lundstedt, Emily A., Davis, Rebecca M., Kahne, Daniel, and Ruiz, Natividad. Tue .
"Combining Mutations That Inhibit Two Distinct Steps of the ATP Hydrolysis Cycle Restores Wild-Type Function in the Lipopolysaccharide Transporter and Shows that ATP Binding Triggers Transport". United States. https://doi.org/10.1128/mbio.01931-19. https://www.osti.gov/servlets/purl/1569912.
@article{osti_1569912,
title = {Combining Mutations That Inhibit Two Distinct Steps of the ATP Hydrolysis Cycle Restores Wild-Type Function in the Lipopolysaccharide Transporter and Shows that ATP Binding Triggers Transport},
author = {Simpson, Brent W. and Pahil, Karanbir S. and Owens, Tristan W. and Lundstedt, Emily A. and Davis, Rebecca M. and Kahne, Daniel and Ruiz, Natividad},
abstractNote = {ATP-binding cassette (ABC) transporters constitute a large family of proteins present in all domains of life. They are powered by dynamic ATPases that harness energy from binding and hydrolyzing ATP through a cycle that involves the closing and reopening of their two ATP-binding domains. The LptB2FGC exporter is an essential ABC transporter that assembles lipopolysaccharides (LPS) on the surface of Gram-negative bacteria to form a permeability barrier against many antibiotics. LptB2FGC extracts newly synthesized LPS molecules from the inner membrane and powers their transport across the periplasm and through the outer membrane. How LptB2FGC functions remains poorly understood. Here, we show that the C-terminal domain of the dimeric LptB ATPase is essential for LPS transport in Escherichia coli. Specific changes in the C-terminal domain of LptB cause LPS transport defects that can be repaired by intragenic suppressors altering the ATP-binding domains. Surprisingly, we found that each of two lethal changes in the ATP-binding and C-terminal domains of LptB, when present in combined form, suppressed the defects associated with the other to restore LPS transport to wild-type levels both in vivo and in vitro. We present biochemical evidence explaining the effect that each of these mutations has on LptB function and how the observed cosuppression results from the opposing lethal effects these changes have on the dimerization state of the LptB ATPase. We therefore propose that these sites modulate the closing and reopening of the LptB dimer, providing insight into how the LptB2FGC transporter cycles to export LPS to the cell surface and how to inhibit this essential envelope biogenesis process.},
doi = {10.1128/mbio.01931-19},
journal = {mBio (Online)},
number = 4,
volume = 10,
place = {United States},
year = {Tue Aug 20 00:00:00 EDT 2019},
month = {Tue Aug 20 00:00:00 EDT 2019}
}
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