Functional plasticity of antibacterial EndoU toxins
Abstract
Abstract Bacteria use several different secretion systems to deliver toxic EndoU ribonucleases into neighboring cells. Here, we present the first structure of a prokaryotic EndoU toxin in complex with its cognate immunity protein. The contact‐dependent growth inhibition toxin CdiA‐CT STECO31 from Escherichia coli STEC_O31 adopts the eukaryotic EndoU fold and shares greatest structural homology with the nuclease domain of coronavirus Nsp15. The toxin contains a canonical His‐His‐Lys catalytic triad in the same arrangement as eukaryotic EndoU domains, but lacks the uridylate‐specific ribonuclease activity that characterizes the superfamily. Comparative sequence analysis indicates that bacterial EndoU domains segregate into at least three major clades based on structural variations in the N‐terminal subdomain. Representative EndoU nucleases from clades I and II degrade tRNA molecules with little specificity. In contrast, CdiA‐CT STECO31 and other clade III toxins are specific anticodon nucleases that cleave tRNA Glu between nucleotides C37 and m 2 A38. These findings suggest that the EndoU fold is a versatile scaffold for the evolution of novel substrate specificities. Such functional plasticity may account for the widespread use of EndoU effectors by diverse inter‐bacterial toxin delivery systems.
- Authors:
-
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Univ. of California, Santa Barbara, CA (United States)
- Uppsala Univ., Uppsala (Sweden)
- Univ. of California, Irvine, CA (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1491848
- Alternate Identifier(s):
- OSTI ID: 1464280
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Microbiology
- Additional Journal Information:
- Journal Volume: 109; Journal Issue: 4; Journal ID: ISSN 0950-382X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Michalska, Karolina, Nhan, Dinh Quan, Willett, Julia L. E., Stols, Lucy M., Eschenfeldt, William H., Jones, Allison M., Nguyen, Josephine Y., Koskiniemi, Sanna, Low, David A., Goulding, Celia W., Joachimiak, Andrzej, and Hayes, Christopher S. Functional plasticity of antibacterial EndoU toxins. United States: N. p., 2018.
Web. doi:10.1111/mmi.14007.
Michalska, Karolina, Nhan, Dinh Quan, Willett, Julia L. E., Stols, Lucy M., Eschenfeldt, William H., Jones, Allison M., Nguyen, Josephine Y., Koskiniemi, Sanna, Low, David A., Goulding, Celia W., Joachimiak, Andrzej, & Hayes, Christopher S. Functional plasticity of antibacterial EndoU toxins. United States. https://doi.org/10.1111/mmi.14007
Michalska, Karolina, Nhan, Dinh Quan, Willett, Julia L. E., Stols, Lucy M., Eschenfeldt, William H., Jones, Allison M., Nguyen, Josephine Y., Koskiniemi, Sanna, Low, David A., Goulding, Celia W., Joachimiak, Andrzej, and Hayes, Christopher S. Wed .
"Functional plasticity of antibacterial EndoU toxins". United States. https://doi.org/10.1111/mmi.14007. https://www.osti.gov/servlets/purl/1491848.
@article{osti_1491848,
title = {Functional plasticity of antibacterial EndoU toxins},
author = {Michalska, Karolina and Nhan, Dinh Quan and Willett, Julia L. E. and Stols, Lucy M. and Eschenfeldt, William H. and Jones, Allison M. and Nguyen, Josephine Y. and Koskiniemi, Sanna and Low, David A. and Goulding, Celia W. and Joachimiak, Andrzej and Hayes, Christopher S.},
abstractNote = {Abstract Bacteria use several different secretion systems to deliver toxic EndoU ribonucleases into neighboring cells. Here, we present the first structure of a prokaryotic EndoU toxin in complex with its cognate immunity protein. The contact‐dependent growth inhibition toxin CdiA‐CT STECO31 from Escherichia coli STEC_O31 adopts the eukaryotic EndoU fold and shares greatest structural homology with the nuclease domain of coronavirus Nsp15. The toxin contains a canonical His‐His‐Lys catalytic triad in the same arrangement as eukaryotic EndoU domains, but lacks the uridylate‐specific ribonuclease activity that characterizes the superfamily. Comparative sequence analysis indicates that bacterial EndoU domains segregate into at least three major clades based on structural variations in the N‐terminal subdomain. Representative EndoU nucleases from clades I and II degrade tRNA molecules with little specificity. In contrast, CdiA‐CT STECO31 and other clade III toxins are specific anticodon nucleases that cleave tRNA Glu between nucleotides C37 and m 2 A38. These findings suggest that the EndoU fold is a versatile scaffold for the evolution of novel substrate specificities. Such functional plasticity may account for the widespread use of EndoU effectors by diverse inter‐bacterial toxin delivery systems.},
doi = {10.1111/mmi.14007},
journal = {Molecular Microbiology},
number = 4,
volume = 109,
place = {United States},
year = {Wed Jun 20 00:00:00 EDT 2018},
month = {Wed Jun 20 00:00:00 EDT 2018}
}
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