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.
José E. González-Pastor 1,Errett C. Hobbs 2,Richard Losick 2*
1 Department of Molecular and Cellular Biology, The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA; Present Address: Centro Nacional de Biotecnología CSIC, Campus de Cantoblanco, 28049 Madrid, Spain. 2 Department of Molecular and Cellular Biology, The Biological Laboratories, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.
* To whom correspondence should be addressed. E-mail: losick{at}mcb.harvard.edu.
Spore formation by the bacterium Bacillus subtilis is an elaboratedevelopmental process that is triggered by nutrient limitation.Here we report that cells that have entered the pathway to sporulateproduce and export a killing factor and a novel signaling proteinthat act cooperatively to block sister cells from sporulatingand to cause them to lyse. The sporulating cells feed on thenutrients thereby released, allowing them to keep growing ratherthan completing morphogenesis. We propose that sporulation isa stress-response pathway of last resort and that B. subtilisdelays a commitment to spore formation by cannibalizing itssiblings.
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
Hanna Engelberg-Kulka and Ronen Hazan (25 July 2003) Science301 (5632), 467.
[DOI: 10.1126/science.1088051] |Summary »|Full Text »|PDF »
{sigma}X Is Involved in Controlling Bacillus subtilis Biofilm Architecture through the AbrB Homologue Abh.
E. J. Murray, M. A. Strauch, and N. R. Stanley-Wall (2009)
J. Bacteriol.
191, 6822-6832
|Abstract »|Full Text »|PDF »
Lack of A-factor Production Induces the Expression of Nutrient Scavenging and Stress-related Proteins in Streptomyces griseus.
Z. Birko, M. Swiatek, E. Szajli, K. F. Medzihradszky, E. Vijgenboom, A. Penyige, J. Keseru, G. P. van Wezel, and S. Biro (2009)
Mol. Cell. Proteomics
8, 2396-2403
|Abstract »|Full Text »|PDF »
Paenibacillus dendritiformis Bacterial Colony Growth Depends on Surfactant but Not on Bacterial Motion.
A. Be'er, R. S. Smith, H. P. Zhang, E.-L. Florin, S. M. Payne, and H. L. Swinney (2009)
J. Bacteriol.
191, 5758-5764
|Abstract »|Full Text »|PDF »
Plasmid pAMS1-Encoded, Bacteriocin-Related "Siblicide" in Enterococcus faecalis.
C. M. Sedgley, D. B. Clewell, and S. E. Flannagan (2009)
J. Bacteriol.
191, 3183-3188
|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.
Oscillations in continuous culture populations of Streptococcus pneumoniae: population dynamics and the evolution of clonal suicide.
O. E Cornejo, D. E Rozen, R. M May, and B. R Levin (2009)
Proc R Soc B
276, 999-1008
|Abstract »|Full Text »|PDF »
Deadly competition between sibling bacterial colonies.
A. Be'er, H. P. Zhang, E.-L. Florin, S. M. Payne, E. Ben-Jacob, and H. L. Swinney (2009)
PNAS
106, 428-433
|Abstract »|Full Text »|PDF »
Development and Application of Flow-Cytometric Techniques for Analyzing and Sorting Endospore-Forming Clostridia.
B. P. Tracy, S. M. Gaida, and E. T. Papoutsakis (2008)
Appl. Envir. Microbiol.
74, 7497-7506
|Abstract »|Full Text »|PDF »
Effect of Temperature on the Cannibalistic Behavior of Bacillus subtilis.
S. K. Nandy, V. Prasad, and K. V. Venkatesh (2008)
Appl. Envir. Microbiol.
74, 7427-7430
|Abstract »|Full Text »|PDF »
Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis.
A. V. Banse, A. Chastanet, L. Rahn-Lee, E. C. Hobbs, and R. Losick (2008)
PNAS
105, 15547-15552
|Abstract »|Full Text »|PDF »
Two distinct arabinofuranosidases contribute to arabino-oligosaccharide degradation in Bacillus subtilis.
J. M. Inacio, I. L. Correia, and I. de Sa-Nogueira (2008)
Microbiology
154, 2719-2729
|Abstract »|Full Text »|PDF »
Regulation of Autolysis-Dependent Extracellular DNA Release by Enterococcus faecalis Extracellular Proteases Influences Biofilm Development.
V. C. Thomas, L. R. Thurlow, D. Boyle, and L. E. Hancock (2008)
J. Bacteriol.
190, 5690-5698
|Abstract »|Full Text »|PDF »
Hydrogen Peroxide Linked to Lysine Oxidase Activity Facilitates Biofilm Differentiation and Dispersal in Several Gram-Negative Bacteria.
A. Mai-Prochnow, P. Lucas-Elio, S. Egan, T. Thomas, J. S. Webb, A. Sanchez-Amat, and S. Kjelleberg (2008)
J. Bacteriol.
190, 5493-5501
|Abstract »|Full Text »|PDF »
Recovery of Spores from Thermophilic Dairy Bacilli and Effects of Their Surface Characteristics on Attachment to Different Surfaces.
R. B. Seale, S. H. Flint, A. J. McQuillan, and P. J. Bremer (2008)
Appl. Envir. Microbiol.
74, 731-737
|Abstract »|Full Text »|PDF »
Abh and AbrB Control of Bacillus subtilis Antimicrobial Gene Expression.
M. A. Strauch, B. G. Bobay, J. Cavanagh, F. Yao, A. Wilson, and Y. Le Breton (2007)
J. Bacteriol.
189, 7720-7732
|Abstract »|Full Text »|PDF »
A Linear Pentapeptide Is a Quorum-Sensing Factor Required for mazEF-Mediated Cell Death in Escherichia coli.
I. Kolodkin-Gal, R. Hazan, A. Gaathon, S. Carmeli, and H. Engelberg-Kulka (2007)
Science
318, 652-655
|Abstract »|Full Text »|PDF »
Model-based Definition of Population Heterogeneity and Its Effects on Metabolism in Sporulating Bacillus subtilis.
M. Morohashi, Y. Ohashi, S. Tani, K. Ishii, M. Itaya, H. Nanamiya, F. Kawamura, M. Tomita, and T. Soga (2007)
J. Biochem.
142, 183-191
|Abstract »|Full Text »|PDF »
Novel Iso-branched Ether Lipids as Specific Markers of Developmental Sporulation in the Myxobacterium Myxococcus xanthus.
M. W. Ring, G. Schwar, V. Thiel, J. S. Dickschat, R. M. Kroppenstedt, S. Schulz, and H. B. Bode (2006)
J. Biol. Chem.
281, 36691-36700
|Abstract »|Full Text »|PDF »
Ecological Advantages of Autolysis during the Development and Dispersal of Pseudoalteromonas tunicata Biofilms.
A. Mai-Prochnow, J. S. Webb, B. C. Ferrari, and S. Kjelleberg (2006)
Appl. Envir. Microbiol.
72, 5414-5420
|Abstract »|Full Text »|PDF »
Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis.
Phosphate Starvation Induces the Sporulation Killing Factor of Bacillus subtilis..
N. E. E. Allenby, C. A. Watts, G. Homuth, Z. Pragai, A. Wipat, A. C. Ward, and C. R. Harwood (2006)
J. Bacteriol.
188, 5299-5303
|Abstract »|Full Text »|PDF »
Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells..
L. Lugini, P. Matarrese, A. Tinari, F. Lozupone, C. Federici, E. Iessi, M. Gentile, F. Luciani, G. Parmiani, L. Rivoltini, et al. (2006)
Cancer Res.
66, 3629-3638
|Abstract »|Full Text »|PDF »
Spo0A-Dependent Activation of an Extended -10 Region Promoter in Bacillus subtilis.
G. Chen, A. Kumar, T. H. Wyman, and C. P. Moran Jr. (2006)
J. Bacteriol.
188, 1411-1418
|Abstract »|Full Text »|PDF »
Cell population heterogeneity during growth of Bacillus subtilis.
Genome-Wide Transcriptional Analysis of the Phosphate Starvation Stimulon of Bacillus subtilis.
N. E. E. Allenby, N. O'Connor, Z. Pragai, A. C. Ward, A. Wipat, and C. R. Harwood (2005)
J. Bacteriol.
187, 8063-8080
|Abstract »|Full Text »|PDF »
A death round affecting a young compartmentalized mycelium precedes aerial mycelium dismantling in confluent surface cultures of Streptomyces antibioticus.
A. Manteca, M. Fernandez, and J. Sanchez (2005)
Microbiology
151, 3689-3697
|Abstract »|Full Text »|PDF »
mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria.
H. Engelberg-Kulka, R. Hazan, and S. Amitai (2005)
J. Cell Sci.
118, 4327-4332
|Abstract »|Full Text »|PDF »
Independent and Interchangeable Multimerization Domains of the AbrB, Abh, and SpoVT Global Regulatory Proteins.
Tricksy Business: Transcriptome Analysis Reveals the Involvement of Thioredoxin A in Redox Homeostasis, Oxidative Stress, Sulfur Metabolism, and Cellular Differentiation in Bacillus subtilis.
W. K. Smits, J.-Y. F. Dubois, S. Bron, J. M. van Dijl, and O. P. Kuipers (2005)
J. Bacteriol.
187, 3921-3930
|Abstract »|Full Text »|PDF »
The selective advantage of microbial fratricide.
M. S. Gilmore and W. Haas (2005)
PNAS
102, 8401-8402
|Full Text »|PDF »
From The Cover: Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: Genetic requirements.
S. Guiral, T. J. Mitchell, B. Martin, and J.-P. Claverys (2005)
PNAS
102, 8710-8715
|Abstract »|Full Text »|PDF »
RECOMBINANT LARVICIDAL BACTERIA WITH MARKEDLY IMPROVED EFFICACY AGAINST CULEX VECTORS OF WEST NILE VIRUS.
H.-W. PARK, D. K. BIDESHI, M. C. WIRTH, J. J. JOHNSON, W. E. WALTON, and B. A. FEDERICI (2005)
Am J Trop Med Hyg
72, 732-738
|Abstract »|Full Text »|PDF »
Genes Involved in SkfA Killing Factor Production Protect a Bacillus subtilis Lipase against Proteolysis.
H. Westers, P. G. Braun, L. Westers, H. Antelmann, M. Hecker, J. D. H. Jongbloed, H. Yoshikawa, T. Tanaka, J. M. van Dijl, and W. J. Quax (2005)
Appl. Envir. Microbiol.
71, 1899-1908
|Abstract »|Full Text »|PDF »
The Rok Protein of Bacillus subtilis Represses Genes for Cell Surface and Extracellular Functions.
M. Albano, W. K. Smits, L. T. Y. Ho, B. Kraigher, I. Mandic-Mulec, O. P. Kuipers, and D. Dubnau (2005)
J. Bacteriol.
187, 2010-2019
|Abstract »|Full Text »|PDF »
High- and Low-Threshold Genes in the Spo0A Regulon of Bacillus subtilis.
M. Fujita, J. E. Gonzalez-Pastor, and R. Losick (2005)
J. Bacteriol.
187, 1357-1368
|Abstract »|Full Text »|PDF »
Mitochondrial fission proteins regulate programmed cell death in yeast.
Y. Fannjiang, W.-C. Cheng, S. J. Lee, B. Qi, J. Pevsner, J. M. McCaffery, R. B. Hill, G. Basanez, and J. M. Hardwick (2004)
Genes & Dev.
18, 2785-2797
|Abstract »|Full Text »|PDF »
Visualization of Differential Gene Expression by Improved Cyan Fluorescent Protein and Yellow Fluorescent Protein Production in Bacillus subtilis.
J.-W. Veening, W. K. Smits, L. W. Hamoen, J. D. H. Jongbloed, and O. P. Kuipers (2004)
Appl. Envir. Microbiol.
70, 6809-6815
|Abstract »|Full Text »|PDF »
Hetero- and Autoprocessing of the Extracellular Metalloprotease (Mpr) in Bacillus subtilis.
C. H. Park, S. J. Lee, S. G. Lee, W. S. Lee, and S. M. Byun (2004)
J. Bacteriol.
186, 6457-6464
|Abstract »|Full Text »|PDF »
Anaerobic Growth of Bacillus mojavensis and Bacillus subtilis Requires Deoxyribonucleosides or DNA.
M. J. Folmsbee, M. J. McInerney, and D. P. Nagle (2004)
Appl. Envir. Microbiol.
70, 5252-5257
|Abstract »|Full Text »|PDF »
Biofilm Development and Cell Death in the Marine Bacterium Pseudoalteromonas tunicata.
A. Mai-Prochnow, F. Evans, D. Dalisay-Saludes, S. Stelzer, S. Egan, S. James, J. S. Webb, and S. Kjelleberg (2004)
Appl. Envir. Microbiol.
70, 3232-3238
|Abstract »|Full Text »|PDF »
Escherichia coli mazEF-Mediated Cell Death Is Triggered by Various Stressful Conditions.
R. Hazan, B. Sat, and H. Engelberg-Kulka (2004)
J. Bacteriol.
186, 3663-3669
|Abstract »|Full Text »|PDF »
Subtilosin Production by Two Bacillus subtilis Subspecies and Variance of the sbo-alb Cluster.
T. Stein, S. Dusterhus, A. Stroh, and K.-D. Entian (2004)
Appl. Envir. Microbiol.
70, 2349-2353
|Abstract »|Full Text »|PDF »
Compartmentalization of Gene Expression during Sporulation of Bacillus subtilis Is Compromised in Mutants Blocked at Stage III of Sporulation.