An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells
Abstract
Type VI secretion (T6S) influences the composition of microbial communities by catalyzing the delivery of toxins between adjacent bacterial cells. Here, we demonstrate that a T6S integral membrane toxin from Pseudomonas aeruginosa, Tse6, acts on target cells by degrading the universally essential dinucleotides NAD+ and NADP+. Structural analyses of Tse6 show that it resembles mono-ADP-ribosyltransferase proteins, such as diphtheria toxin, with the exception of a unique loop that both excludes proteinaceous ADP-ribose acceptors and contributes to hydrolysis. We find that entry of Tse6 into target cells requires its binding to an essential housekeeping protein, translation elongation factor Tu (EF-Tu). These proteins participate in a larger assembly that additionally directs toxin export and provides chaperone activity. Lastly, visualization of this complex by electron microscopy defines the architecture of a toxin-loaded T6S apparatus and provides mechanistic insight into intercellular membrane protein delivery between bacteria.
- Authors:
-
- Univ. of Washington, Seattle, WA (United States)
- Max Planck Institute of Molecular Physiology, Dortmund (Germany)
- Univ. of Maryland, Baltimore, MD (United States)
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Univ. of Washington, Seattle, WA (United States); Howard Hughes Medical Institute, Seattle, WA (United States)
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1340347
- Report Number(s):
- BNL-112066-2016-JA
Journal ID: ISSN 0092-8674
- Grant/Contract Number:
- SC00112704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cell
- Additional Journal Information:
- Journal Volume: 163; Journal Issue: 3; Journal ID: ISSN 0092-8674
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE
Citation Formats
Whitney, John C., Quentin, Dennis, Sawai, Shin, LeRoux, Michele, Harding, Brittany N., Ledvina, Hannah E., Tran, Bao Q., Robinson, Howard, Goo, Young Ah, Goodlett, David R., Raunser, Stefan, and Mougous, Joseph D. An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells. United States: N. p., 2015.
Web. doi:10.1016/j.cell.2015.09.027.
Whitney, John C., Quentin, Dennis, Sawai, Shin, LeRoux, Michele, Harding, Brittany N., Ledvina, Hannah E., Tran, Bao Q., Robinson, Howard, Goo, Young Ah, Goodlett, David R., Raunser, Stefan, & Mougous, Joseph D. An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells. United States. https://doi.org/10.1016/j.cell.2015.09.027
Whitney, John C., Quentin, Dennis, Sawai, Shin, LeRoux, Michele, Harding, Brittany N., Ledvina, Hannah E., Tran, Bao Q., Robinson, Howard, Goo, Young Ah, Goodlett, David R., Raunser, Stefan, and Mougous, Joseph D. Thu .
"An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells". United States. https://doi.org/10.1016/j.cell.2015.09.027. https://www.osti.gov/servlets/purl/1340347.
@article{osti_1340347,
title = {An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells},
author = {Whitney, John C. and Quentin, Dennis and Sawai, Shin and LeRoux, Michele and Harding, Brittany N. and Ledvina, Hannah E. and Tran, Bao Q. and Robinson, Howard and Goo, Young Ah and Goodlett, David R. and Raunser, Stefan and Mougous, Joseph D.},
abstractNote = {Type VI secretion (T6S) influences the composition of microbial communities by catalyzing the delivery of toxins between adjacent bacterial cells. Here, we demonstrate that a T6S integral membrane toxin from Pseudomonas aeruginosa, Tse6, acts on target cells by degrading the universally essential dinucleotides NAD+ and NADP+. Structural analyses of Tse6 show that it resembles mono-ADP-ribosyltransferase proteins, such as diphtheria toxin, with the exception of a unique loop that both excludes proteinaceous ADP-ribose acceptors and contributes to hydrolysis. We find that entry of Tse6 into target cells requires its binding to an essential housekeeping protein, translation elongation factor Tu (EF-Tu). These proteins participate in a larger assembly that additionally directs toxin export and provides chaperone activity. Lastly, visualization of this complex by electron microscopy defines the architecture of a toxin-loaded T6S apparatus and provides mechanistic insight into intercellular membrane protein delivery between bacteria.},
doi = {10.1016/j.cell.2015.09.027},
journal = {Cell},
number = 3,
volume = 163,
place = {United States},
year = {Thu Oct 08 00:00:00 EDT 2015},
month = {Thu Oct 08 00:00:00 EDT 2015}
}
Web of Science
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journal, April 2020
- Flaugnatti, Nicolas; Rapisarda, Chiara; Rey, Martial
- The EMBO Journal, Vol. 39, Issue 11
A phospholipase A 1 antibacterial Type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery: Phospholipase A 1 antibacterial T6SS effector
journal, February 2016
- Flaugnatti, Nicolas; Le, Thi Thu Hang; Canaan, Stéphane
- Molecular Microbiology, Vol. 99, Issue 6
Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species
journal, March 2016
- Chatzidaki-Livanis, Maria; Geva-Zatorsky, Naama; Comstock, Laurie E.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 13
Type VI secretion system: a modular toolkit for bacterial dominance
journal, November 2019
- Jana, Biswanath; Salomon, Dor
- Future Microbiology, Vol. 14, Issue 16
PAAR‐Rhs proteins harbor various C‐terminal toxins to diversify the antibacterial pathways of type VI secretion systems
journal, December 2016
- Ma, Jiale; Sun, Min; Dong, Wenyang
- Environmental Microbiology, Vol. 19, Issue 1
Type VI Secretion Effectors: Methodologies and Biology
journal, June 2017
- Lien, Yun-Wei; Lai, Erh-Min
- Frontiers in Cellular and Infection Microbiology, Vol. 7
A High-Throughput Interbacterial Competition Screen Identifies ClpAP in Enhancing Recipient Susceptibility to Type VI Secretion System-Mediated Attack by Agrobacterium tumefaciens
journal, February 2020
- Lin, Hsiao-Han; Yu, Manda; Sriramoju, Manoj Kumar
- Frontiers in Microbiology, Vol. 10
The RES domain toxins of RES-Xre toxin-antitoxin modules induce cell stasis by degrading NAD +: The RES toxin degrades intracellular NAD+
journal, November 2018
- Skjerning, Ragnhild Bager; Senissar, Meriem; Winther, Kristoffer S.
- Molecular Microbiology, Vol. 111, Issue 1
The opportunistic pathogen Stenotrophomonas maltophilia utilizes a type IV secretion system for interbacterial killing
journal, February 2019
- Bayer-Santos, Ethel; Cenens, William; Matsuyama, Bruno Yasui
- PLOS Pathogens
Discovery of a Pseudomonas aeruginosa Type VI secretion system toxin targeting bacterial protein synthesis using a global genomics approach
posted_content, August 2019
- Nolan, Laura M.; Cain, Amy K.; Manoli, Eleni
- BioRxiv
A proposed chaperone of the bacterial type VI secretion system functions to constrain a self-identity protein
journal, November 2017
- Zepeda-Rivera, Martha A.; Saak, Christina C.; Gibbs, Karine A.
- Journal of Bacteriology
A Type VI Secretion System Trans-Kingdom Effector Is Required for the Delivery of a Novel Antibacterial Toxin in Pseudomonas aeruginosa
journal, June 2019
- Berni, Benjamin; Soscia, Chantal; Djermoun, Sarah
- Frontiers in Microbiology, Vol. 10
Influence of 6-aminonicotinamide (6AN) on Leishmania promastigotes evaluated by metabolomics: Beyond the pentose phosphate pathway
journal, October 2018
- Almugadam, Shawgi Hago; Trentini, Alessandro; Maritati, Martina
- Chemico-Biological Interactions, Vol. 294
Vibrio cholerae type 6 secretion system effector trafficking in target bacterial cells
journal, August 2017
- Ho, Brian T.; Fu, Yang; Dong, Tao G.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 35
Type VI secretion system MIX‐effectors carry both antibacterial and anti‐eukaryotic activities
journal, September 2017
- Ray, Ann; Schwartz, Nika; Souza Santos, Marcela
- EMBO reports, Vol. 18, Issue 11
An onboard checking mechanism ensures effector delivery of the type VI secretion system in Vibrio cholerae
journal, October 2019
- Liang, Xiaoye; Kamal, Fatima; Pei, Tong-Tong
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 46
Phosphorylation decelerates conformational dynamics in bacterial translation elongation factors
journal, March 2018
- Talavera, Ariel; Hendrix, Jelle; Versées, Wim
- Science Advances, Vol. 4, Issue 3
Causalities of war: The connection between type VI secretion system and microbiota
journal, January 2020
- Allsopp, Luke P.; Bernal, Patricia; Nolan, Laura M.
- Cellular Microbiology, Vol. 22, Issue 3
The tuberculosis necrotizing toxin is an NAD+ and NADP+ glycohydrolase with distinct enzymatic properties
text, January 2019
- Tak, Uday; Vlach, Jiri; Garza-Garcia, Acely
- The Francis Crick Institute