An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells

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.

doi:10.1016/j.cell.2015.09.027

Title: An interbacterial NAD(P)⁺ glycohydrolase toxin requires elongation factor Tu for delivery to target cells

Journal Article · Thu Oct 08 00:00:00 EDT 2015 · Cell

DOI:https://doi.org/10.1016/j.cell.2015.09.027· OSTI ID:1340347

Whitney, John C. ^[1]; Quentin, Dennis ^[2]; Sawai, Shin ^[1]; LeRoux, Michele ^[1]; Harding, Brittany N. ^[1]; Ledvina, Hannah E. ^[1]; Tran, Bao Q. ^[3]; Robinson, Howard ^[4]; Goo, Young Ah ^[3]; Goodlett, David R. ^[3]; Raunser, Stefan ^[2]; Mougous, Joseph D. ^[5]

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)

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.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC00112704

OSTI ID:: 1340347

Report Number(s):: BNL-112066-2016-JA

Journal Information:: Cell, Vol. 163, Issue 3; ISSN 0092-8674

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 145 works

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A proposed chaperone of the bacterial type VI secretion system functions to constrain a self-identity protein Zepeda-Rivera, Martha A.; Saak, Christina C.; Gibbs, Karine A. Journal of Bacteriology https://doi.org/10.1101/213785	journal	November 2017
A Type VI Secretion System Trans-Kingdom Effector Is Required for the Delivery of a Novel Antibacterial Toxin in Pseudomonas aeruginosa Berni, Benjamin; Soscia, Chantal; Djermoun, Sarah Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01218	journal	June 2019
Influence of 6-aminonicotinamide (6AN) on Leishmania promastigotes evaluated by metabolomics: Beyond the pentose phosphate pathway Almugadam, Shawgi Hago; Trentini, Alessandro; Maritati, Martina Chemico-Biological Interactions, Vol. 294 https://doi.org/10.1016/j.cbi.2018.08.014	journal	October 2018
Type VI secretion system MIX‐effectors carry both antibacterial and anti‐eukaryotic activities Ray, Ann; Schwartz, Nika; Souza Santos, Marcela EMBO reports, Vol. 18, Issue 11 https://doi.org/10.15252/embr.201744226	journal	September 2017
An onboard checking mechanism ensures effector delivery of the type VI secretion system in Vibrio cholerae Liang, Xiaoye; Kamal, Fatima; Pei, Tong-Tong Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1914202116	journal	October 2019
Phosphorylation decelerates conformational dynamics in bacterial translation elongation factors Talavera, Ariel; Hendrix, Jelle; Versées, Wim Science Advances, Vol. 4, Issue 3 https://doi.org/10.1126/sciadv.aap9714	journal	March 2018
Causalities of war: The connection between type VI secretion system and microbiota Allsopp, Luke P.; Bernal, Patricia; Nolan, Laura M. Cellular Microbiology, Vol. 22, Issue 3 https://doi.org/10.1111/cmi.13153	journal	January 2020
The tuberculosis necrotizing toxin is an NAD+ and NADP+ glycohydrolase with distinct enzymatic properties Tak, Uday; Vlach, Jiri; Garza-Garcia, Acely The Francis Crick Institute https://doi.org/10.25418/crick.11409831	text	January 2019

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