Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 318 (5850): 652-655

Copyright © 2007 by the American Association for the Advancement of Science

A Linear Pentapeptide Is a Quorum-Sensing Factor Required for mazEF-Mediated Cell Death in Escherichia coli

Ilana Kolodkin-Gal,1 Ronen Hazan,1* Ariel Gaathon,2 Shmuel Carmeli,3 Hanna Engelberg-Kulka1{dagger}

Abstract: mazEF is a toxin-antitoxin module located on many bacterial chromosomes, including those of pathogens. Here, we report that Escherichia coli mazEF-mediated cell death is a population phenomenon requiring a quorum-sensing molecule that we call the extracellular death factor (EDF). Structural analysis revealed that EDF is a linear pentapeptide, Asn-Asn-Trp-Asn-Asn. Each of the five amino acids of EDF is important for its activity.

1 Department of Molecular Biology, Hebrew University–Hadassah Medical School, Jerusalem 91120, Israel.
2 Core Research Facility, Hebrew University–Hadassah Medical School, Jerusalem 91120, Israel.
3 School of Chemistry, Tel Aviv University, Tel Aviv 69978, Israel.

* Present address: Massachusetts General Hospital, Department of Surgery, Harvard Medical School, Boston, MA 02114, USA.

{dagger} To whom correspondence should be addressed. E-mail: hanita{at}

Programming stress-induced altruistic death in engineered bacteria.
Y. Tanouchi, A. Pai, N. E. Buchler, and L. You (2014)
Mol Syst Biol 8, 626
   Abstract »    Full Text »    PDF »
A Moderate Toxin, GraT, Modulates Growth Rate and Stress Tolerance of Pseudomonas putida.
H. Tamman, A. Ainelo, K. Ainsaar, and R. Horak (2014)
J. Bacteriol. 196, 157-169
   Abstract »    Full Text »    PDF »
Novel Quorum-Sensing Peptides Mediating Interspecies Bacterial Cell Death.
S. Kumar, I. Kolodkin-Gal, and H. Engelberg-Kulka (2013)
mBio 4, e00314-13
   Abstract »    Full Text »    PDF »
Hypothesis: Bacteria Control Host Appetites.
V. Norris, F. Molina, and A. T. Gewirtz (2013)
J. Bacteriol. 195, 411-416
   Abstract »    Full Text »    PDF »
Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides.
E. Wynendaele, A. Bronselaer, J. Nielandt, M. D'Hondt, S. Stalmans, N. Bracke, F. Verbeke, C. Van De Wiele, G. De Tre, and B. De Spiegeleer (2013)
Nucleic Acids Res. 41, D655-D659
   Abstract »    Full Text »    PDF »
Toxin-Antitoxin Genes of the Gram-Positive Pathogen Streptococcus pneumoniae: So Few and Yet So Many.
W. T. Chan, I. Moreno-Cordoba, C. C. Yeo, and M. Espinosa (2012)
Microbiol. Mol. Biol. Rev. 76, 773-791
   Abstract »    Full Text »    PDF »
BapE DNA endonuclease induces an apoptotic-like response to DNA damage in Caulobacter.
J. Bos, A. A. Yakhnina, and Z. Gitai (2012)
PNAS 109, 18096-18101
   Abstract »    Full Text »    PDF »
Clostridium difficile MazF Toxin Exhibits Selective, Not Global, mRNA Cleavage.
F. P. Rothenbacher, M. Suzuki, J. M. Hurley, T. J. Montville, T. J. Kirn, M. Ouyang, and N. A. Woychik (2012)
J. Bacteriol. 194, 3464-3474
   Abstract »    Full Text »    PDF »
RelE-Mediated Dormancy Is Enhanced at High Cell Density in Escherichia coli.
Y. Tashiro, K. Kawata, A. Taniuchi, K. Kakinuma, T. May, and S. Okabe (2012)
J. Bacteriol. 194, 1169-1176
   Abstract »    Full Text »    PDF »
Evolutionary genome engineering using a restriction-modification system.
Y. Asakura, H. Kojima, and I. Kobayashi (2011)
Nucleic Acids Res. 39, 9034-9046
   Abstract »    Full Text »    PDF »
Genetic Regulation of the yefM-yoeB Toxin-Antitoxin Locus of Streptococcus pneumoniae.
W. T. Chan, C. Nieto, J. A. Harikrishna, S. K. Khoo, R. Y. Othman, M. Espinosa, and C. C. Yeo (2011)
J. Bacteriol. 193, 4612-4625
   Abstract »    Full Text »    PDF »
Transcriptomic Response of Listeria monocytogenes during the Transition to the Long-Term-Survival Phase.
J. Wen, X. Deng, Z. Li, E. G. Dudley, R. C. Anantheswaran, S. J. Knabel, and W. Zhang (2011)
Appl. Envir. Microbiol. 77, 5966-5972
   Abstract »    Full Text »    PDF »
The Chromosomal mazEF Locus of Streptococcus mutans Encodes a Functional Type II Toxin-Antitoxin Addiction System.
M. A. Syed, S. Koyanagi, E. Sharma, M.-C. Jobin, A. F. Yakunin, and C. M. Levesque (2011)
J. Bacteriol. 193, 1122-1130
   Abstract »    Full Text »    PDF »
The role of Escherichia coli YrbB in the lethal action of quinolones.
X. Han, J. Geng, L. Zhang, and T. Lu (2011)
J. Antimicrob. Chemother. 66, 323-331
   Abstract »    Full Text »    PDF »
The Three Vibrio cholerae Chromosome II-Encoded ParE Toxins Degrade Chromosome I following Loss of Chromosome II.
J. Yuan, Y. Yamaichi, and M. K. Waldor (2011)
J. Bacteriol. 193, 611-619
   Abstract »    Full Text »    PDF »
The PIN-domain ribonucleases and the prokaryotic VapBC toxin-antitoxin array.
V. L. Arcus, J. L. McKenzie, J. Robson, and G. M. Cook (2011)
Protein Eng. Des. Sel. 24, 33-40
   Abstract »    Full Text »    PDF »
Noncognate Mycobacterium tuberculosis Toxin-Antitoxins Can Physically and Functionally Interact.
L. Zhu, J. D. Sharp, H. Kobayashi, N. A. Woychik, and M. Inouye (2010)
J. Biol. Chem. 285, 39732-39738
   Abstract »    Full Text »    PDF »
Assembly Dynamics and Stability of the Pneumococcal Epsilon Zeta Antitoxin Toxin (PezAT) System from Streptococcus pneumoniae.
H. Mutschler, J. Reinstein, and A. Meinhart (2010)
J. Biol. Chem. 285, 21797-21806
   Abstract »    Full Text »    PDF »
Structural and Thermodynamic Characterization of Vibrio fischeri CcdB.
N. De Jonge, W. Hohlweg, A. Garcia-Pino, M. Respondek, L. Buts, S. Haesaerts, J. Lah, K. Zangger, and R. Loris (2010)
J. Biol. Chem. 285, 5606-5613
   Abstract »    Full Text »    PDF »
Significant Bias against the ACA Triplet in the tmRNA Sequence of Escherichia coli K-12.
S. Baik, K. Inoue, M. Ouyang, and M. Inouye (2009)
J. Bacteriol. 191, 6157-6166
   Abstract »    Full Text »    PDF »
Paracrine signaling in a bacterium.
D. Lopez, H. Vlamakis, R. Losick, and R. Kolter (2009)
Genes & Dev. 23, 1631-1638
   Abstract »    Full Text »    PDF »
From damaged genome to cell surface: transcriptome changes during bacterial cell death triggered by loss of a restriction-modification gene complex.
Y. Asakura and I. Kobayashi (2009)
Nucleic Acids Res. 37, 3021-3031
   Abstract »    Full Text »    PDF »
Overexpression of MazFSa in Staphylococcus aureus Induces Bacteriostasis by Selectively Targeting mRNAs for Cleavage.
Z. Fu, S. Tamber, G. Memmi, N. P. Donegan, and A. L. Cheung (2009)
J. Bacteriol. 191, 2051-2059
   Abstract »    Full Text »    PDF »
HicA of Escherichia coli Defines a Novel Family of Translation-Independent mRNA Interferases in Bacteria and Archaea.
M. G. Jorgensen, D. P. Pandey, M. Jaskolska, and K. Gerdes (2009)
J. Bacteriol. 191, 1191-1199
   Abstract »    Full Text »    PDF »
Influence of Operator Site Geometry on Transcriptional Control by the YefM-YoeB Toxin-Antitoxin Complex.
S. E. S. Bailey and F. Hayes (2009)
J. Bacteriol. 191, 762-772
   Abstract »    Full Text »    PDF »
The Role of Prophage for Genome Diversification within a Clonal Lineage of Lactobacillus johnsonii: Characterization of the Defective Prophage LJ771.
E. Denou, R. D. Pridmore, M. Ventura, A.-C. Pittet, M.-C. Zwahlen, B. Berger, C. Barretto, J.-M. Panoff, and H. Brussow (2008)
J. Bacteriol. 190, 5806-5813
   Abstract »    Full Text »    PDF »
The Extracellular Death Factor: Physiological and Genetic Factors Influencing Its Production and Response in Escherichia coli.
I. Kolodkin-Gal and H. Engelberg-Kulka (2008)
J. Bacteriol. 190, 3169-3175
   Abstract »    Full Text »    PDF »
Maintenance Forced by a Restriction-Modification System Can Be Modulated by a Region in Its Modification Enzyme Not Essential for Methyltransferase Activity.
S. Ohno, N. Handa, M. Watanabe-Matsui, N. Takahashi, and I. Kobayashi (2008)
J. Bacteriol. 190, 2039-2049
   Abstract »    Full Text »    PDF »
Molecular Control of Bacterial Death and Lysis.
K. C. Rice and K. W. Bayles (2008)
Microbiol. Mol. Biol. Rev. 72, 85-109
   Abstract »    Full Text »    PDF »
MICROBIOLOGY: Deadly Priming.
R. Kolter (2007)
Science 318, 578-579
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882