Convergent Evolution of the Barnase/EndoU/Colicin/RelE (BECR) Fold in Antibacterial tRNase Toxins

Grant C Gucinski; Karolina Michalska; Fernando Garza-Sánchez; William H Eschenfeldt; Lucy Stols; Josephine Y Nguyen; Celia W Goulding; Andrzej Joachimiak; Christopher S Hayes

doi:10.1016/j.str.2019.08.010

Convergent Evolution of the Barnase/EndoU/Colicin/RelE (BECR) Fold in Antibacterial tRNase Toxins

Structure. 2019 Nov 5;27(11):1660-1674.e5. doi: 10.1016/j.str.2019.08.010. Epub 2019 Sep 9.

Authors

Grant C Gucinski¹, Karolina Michalska², Fernando Garza-Sánchez³, William H Eschenfeldt⁴, Lucy Stols⁴, Josephine Y Nguyen³, Celia W Goulding⁵, Andrzej Joachimiak⁶, Christopher S Hayes⁷

Affiliations

¹ Biomolecular Science and Engineering Program, University of California, Santa Barbara, CA, USA.
² Midwest Center for Structural Genomics, Argonne National Laboratory, Lemont, IL, USA; Structural Biology Center, X-ray Science Division, Argonne National Laboratory, Lemont, IL, USA.
³ Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, CA, USA.
⁴ Midwest Center for Structural Genomics, Argonne National Laboratory, Lemont, IL, USA.
⁵ Department of Molecular Biology & Biochemistry, University of California, Irvine, CA, USA; Department of Pharmaceutical Sciences, University of California, Irvine, CA, USA.
⁶ Midwest Center for Structural Genomics, Argonne National Laboratory, Lemont, IL, USA; Structural Biology Center, X-ray Science Division, Argonne National Laboratory, Lemont, IL, USA; Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, IL, USA.
⁷ Biomolecular Science and Engineering Program, University of California, Santa Barbara, CA, USA; Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, CA, USA. Electronic address: chayes@lifesci.ucsb.edu.

Abstract

Contact-dependent growth inhibition (CDI) is a form of interbacterial competition mediated by CdiB-CdiA two-partner secretion systems. CdiA effector proteins carry polymorphic C-terminal toxin domains (CdiA-CT), which are neutralized by specific CdiI immunity proteins to prevent self-inhibition. Here, we present the crystal structures of CdiA-CT⋅CdiI complexes from Klebsiella pneumoniae 342 and Escherichia coli 3006. The toxins adopt related folds that resemble the ribonuclease domain of colicin D, and both are isoacceptor-specific tRNases that cleave the acceptor stem of deacylated tRNA_GAU^Ile. Although the toxins are similar in structure and substrate specificity, CdiA-CT^Kp342 activity requires translation factors EF-Tu and EF-Ts, whereas CdiA-CT^EC3006 is intrinsically active. Furthermore, the corresponding immunity proteins are unrelated in sequence and structure. CdiI^Kp342 forms a dimeric β sandwich, whereas CdiI^EC3006 is an α-solenoid monomer. Given that toxin-immunity genes co-evolve as linked pairs, these observations suggest that the similarities in toxin structure and activity reflect functional convergence.

Keywords: bacterial competition; toxin-antitoxin systems; two-partner secretion; type V secretion system.

Publication types

Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Bacterial Proteins / chemistry*
Bacterial Proteins / genetics
Bacterial Proteins / metabolism
Bacterial Toxins / chemistry*
Bacterial Toxins / genetics
Bacterial Toxins / metabolism
Binding Sites
Colicins / chemistry*
Colicins / genetics
Colicins / metabolism
Escherichia coli
Escherichia coli Proteins / chemistry*
Escherichia coli Proteins / genetics
Escherichia coli Proteins / metabolism
Evolution, Molecular*
Klebsiella pneumoniae / enzymology
Klebsiella pneumoniae / genetics
Membrane Proteins / chemistry*
Membrane Proteins / genetics
Membrane Proteins / metabolism
Protein Binding
RNA, Transfer / chemistry
RNA, Transfer / metabolism
Ribonucleases / chemistry*
Ribonucleases / genetics
Ribonucleases / metabolism
Toxin-Antitoxin Systems*

Substances

Bacterial Proteins
Bacterial Toxins
CdiA protein, E coli
CdiB protein, E coli
Colicins
Escherichia coli Proteins
Membrane Proteins
RelE protein, E coli
RNA, Transfer
Ribonucleases
Bacillus amyloliquefaciens ribonuclease

Abstract

Publication types

MeSH terms

Substances

Grants and funding