Bacterial Programmed Cell Death and Multicellular Behavior in Bacteria

Traditionally, programmed cell death (PCD) is associated with eukaryotic multicellular organisms. However, recently, PCD systems have also been observed in bacteria. Here we review recent research on two kinds of genetic programs that promote bacterial cell death. The first is mediated by mazEF, a toxin–antitoxin module found in the chromosomes of many kinds of bacteria, and mainly studied in Escherichia coli. The second program is found in Bacillus subtilis, in which the skf and sdp operons mediate the death of a subpopulation of sporulating bacterial cells. We relate these two bacterial PCD systems to the ways in which bacterial populations resemble multicellular organisms.

[1]  J. Pincemail,et al.  [Oxidative stress]. , 2007, Revue medicale de Liege.

[2]  M. Inouye,et al.  Insights into the mRNA Cleavage Mechanism by MazF, an mRNA Interferase* , 2005, Journal of Biological Chemistry.

[3]  S. Gottesman,et al.  Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: involvement of the yefM‐yoeB toxin‐antitoxin system , 2004, Molecular microbiology.

[4]  R. Sauer,et al.  The SsrA–SmpB system for protein tagging, directed degradation and ribosome rescue , 2000, Nature Structural Biology.

[5]  K. Lewis,et al.  Programmed Death in Bacteria , 2000, Microbiology and Molecular Biology Reviews.

[6]  S. Korsmeyer,et al.  Cell Death Critical Control Points , 2004, Cell.

[7]  M. Couturier,et al.  Bacterial death by DNA gyrase poisoning. , 1998, Trends in microbiology.

[8]  J. Hoch,et al.  Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay , 1991, Cell.

[9]  G. Salmond,et al.  Quorum sensing: a population-density component in the determination of bacterial phenotype. , 1996, Trends in biochemical sciences.

[10]  K. Gerdes,et al.  Prokaryotic toxin–antitoxin stress response loci , 2005, Nature Reviews Microbiology.

[11]  R. Losick,et al.  A Three-Protein Signaling Pathway Governing Immunity to a Bacterial Cannibalism Toxin , 2006, Cell.

[12]  B. Vanyushin,et al.  Apoptosis in plants: specific features of plant apoptotic cells and effect of various factors and agents. , 2004, International review of cytology.

[13]  S. Bertholet,et al.  Programmed cell death in trypanosomatids and other unicellular organisms. , 2003, International journal for parasitology.

[14]  P. Rather.  Swarmer cell differentiation in Proteus mirabilis. , 2005, Environmental microbiology.

[15]  Ehud Gazit,et al.  The YefM Antitoxin Defines a Family of Natively Unfolded Proteins , 2004, Journal of Biological Chemistry.

[16]  Lode Wyns,et al.  Crystal Structure of the Intrinsically Flexible Addiction Antidote MazE* , 2003, Journal of Biological Chemistry.

[17]  R. Losick,et al.  Cannibalism by Sporulating Bacteria , 2003, Science.

[18]  B. Bassler,et al.  Quorum sensing in bacteria. , 2001, Annual review of microbiology.

[19]  K. Rice,et al.  Death's toolbox: examining the molecular components of bacterial programmed cell death , 2003, Molecular microbiology.

[20]  K. Gerdes,et al.  The Escherichia coli relBE genes belong to a new toxin–antitoxin gene family , 1998, Molecular microbiology.

[21]  I. Tanaka,et al.  Crystal structure of archaeal toxin-antitoxin RelE–RelB complex with implications for toxin activity and antitoxin effects , 2005, Nature Structural &Molecular Biology.

[22]  H. Engelberg-Kulka,et al.  The Escherichia coli mazEF Suicide Module Mediates Thymineless Death , 2003, Journal of bacteriology.

[23]  M. Hengartner.  The biochemistry of apoptosis , 2000, Nature.

[24]  B. Bassler,et al.  Bacterial social engagements. , 2004, Trends in cell biology.

[25]  Finbarr Hayes,et al.  Axe–Txe, a broad‐spectrum proteic toxin–antitoxin system specified by a multidrug‐resistant, clinical isolate of Enterococcus faecium , 2003, Molecular microbiology.

[26]  H. Engelberg-Kulka,et al.  Induction of Escherichia coli Chromosomal mazEF by Stressful Conditions Causes an Irreversible Loss of Viability , 2006, Journal of bacteriology.

[27]  Mitsuhiko Ikura,et al.  MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. , 2003, Molecular cell.

[28]  Lode Wyns,et al.  Toxin-antitoxin modules as bacterial metabolic stress managers. , 2005, Trends in biochemical sciences.

[29]  H. Engelberg-Kulka,et al.  mazEF: a chromosomal toxin-antitoxin module that triggers programmed cell death in bacteria , 2005, Journal of Cell Science.

[30]  J. Ameisen.  Looking for death at the core of life in the light of evolution , 2004, Cell Death and Differentiation.

[31]  Daniel F. Jarosz,et al.  Y‐family DNA polymerases respond to DNA damage‐independent inhibition of replication fork progression , 2006, The EMBO journal.

[32]  K. Gerdes,et al.  Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. , 2003, Journal of molecular biology.

[33]  H. Engelberg-Kulka,et al.  Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1 , 2004, Molecular Genetics and Genomics.

[34]  T. E. Clarke,et al.  INSECT DEFENSES AGAINST VIRUS INFECTION: THE ROLE OF APOPTOSIS , 2003, International reviews of immunology.

[35]  A. Hochman,et al.  Programmed cell death in prokaryotes. , 1997, Critical reviews in microbiology.

[36]  A. Kimchi,et al.  Autophagy as a cell death and tumor suppressor mechanism , 2004, Oncogene.

[37]  H. Engelberg-Kulka,et al.  Programmed Cell Death in Escherichia coli: Some Antibiotics Can Trigger mazEFLethality , 2001, Journal of bacteriology.

[38]  A. Eisenstark,et al.  Thymine metabolism and thymineless death in prokaryotes and eukaryotes. , 1998, Annual review of microbiology.

[39]  J. Ameisen.  The Origin of Programmed Cell Death , 1996, Science.

[40]  K. Rudd,et al.  rpoE, the gene encoding the second heat‐shock sigma factor, sigma E, in Escherichia coli. , 1995, The EMBO journal.

[41]  M. Lemonnier,et al.  Insights into the specificity of RNA cleavage by the Escherichia coli MazF toxin , 2004, FEBS letters.

[42]  H. Engelberg-Kulka,et al.  The Regulation of the Escherichia coli mazEF Promoter Involves an Unusual Alternating Palindrome* , 2001, The Journal of Biological Chemistry.

[43]  W. Hayes.  The genetics of bacteria and their viruses , 1964 .

[44]  C. Szabó.  Mechanisms of cell necrosis. , 2005, Critical care medicine.

[45]  H. Engelberg-Kulka,et al.  MazF-Mediated Cell Death in Escherichia coli: a Point of No Return , 2004, Journal of bacteriology.

[46]  Gholson J. Lyon,et al.  Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria , 2004, Peptides.

[47]  K. Gerdes,et al.  RelE, a global inhibitor of translation, is activated during nutritional stress , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Martin Raff,et al.  Cell suicide for beginners , 1998, Nature.

[49]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[50]  G. Glaser,et al.  MazG – a regulator of programmed cell death in Escherichia coli , 2006, Molecular microbiology.

[51]  E. Greenberg,et al.  Cell-to-cell communication in Escherichia coli and Salmonella typhimurium: they may be talking, but who's listening? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[52]  K. M. Gray,et al.  Intercellular communication and group behavior in bacteria. , 1997, Trends in microbiology.

[53]  R. B. Jensen,et al.  Programmed cell death in bacteria: proteic plasmid stabilization systems , 1995, Molecular microbiology.

[54]  K. Gerdes,et al.  Toxin–antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes , 2005, Nucleic acids research.

[55]  J. Shapiro.  Thinking about bacterial populations as multicellular organisms. , 1998, Annual review of microbiology.

[56]  Finbarr Hayes,et al.  Toxins-Antitoxins: Plasmid Maintenance, Programmed Cell Death, and Cell Cycle Arrest , 2003, Science.

[57]  G. Mittenhuber,et al.  Occurrence of mazEF-like antitoxin/toxin systems in bacteria. , 1999, Journal of molecular microbiology and biotechnology.

[58]  O. Pellegrini,et al.  The Bacillus subtilis ydcDE operon encodes an endoribonuclease of the MazF/PemK family and its inhibitor , 2005, Molecular microbiology.

[59]  D. Kaiser,et al.  How and why bacteria talk to each other , 1993, Cell.

[60]  J. Chaloupka,et al.  Programmed cell death in bacteria , 1996, Folia Microbiologica.

[61]  R. Losick,et al.  The transcriptional profile of early to middle sporulation in Bacillus subtilis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[62]  K. Nakayama,et al.  Thymine starvation-induced structural changes in Escherichia coli DNA. Detection by pulsed field gel electrophoresis and evidence for involvement of homologous recombination. , 1994, Journal of molecular biology.

[63]  S. Burley,et al.  Crystal structure of the MazE/MazF complex: molecular bases of antidote-toxin recognition. , 2003, Molecular cell.

[64]  A. Wilkinson,et al.  Where asymmetry in gene expression originates , 2005, Molecular microbiology.

[65]  H. Engelberg-Kulka,et al.  Bacterial programmed cell death systems as targets for antibiotics. , 2004, Trends in microbiology.

[66]  H. Engelberg-Kulka,et al.  Cannibals Defy Starvation and Avoid Sporulation , 2003, Science.

[67]  G. Barber.  Host defense, viruses and apoptosis , 2001, Cell Death and Differentiation.

[68]  G. McFadden,et al.  Apoptosis: an innate immune response to virus infection. , 1999, Trends in microbiology.

[69]  Bonnie L. Bassler,et al.  Bacterial Small-Molecule Signaling Pathways , 2006, Science.

[70]  M. Inouye,et al.  MazG, a Nucleoside Triphosphate Pyrophosphohydrolase, Interacts with Era, an Essential GTPase in Escherichia coli , 2002, Journal of bacteriology.

[71]  H. Engelberg-Kulka,et al.  Escherichia coli mazEF-Mediated Cell Death Is Triggered by Various Stressful Conditions , 2004, Journal of bacteriology.

[72]  R. Burne,et al.  Characteristics of Streptococcus mutans strains lacking the MazEF and RelBE toxin-antitoxin modules. , 2005, FEMS microbiology letters.

[73]  R. Losick,et al.  An investigation into the compartmentalization of the sporulation transcription factor σE in Bacillus subtilis , 2002, Molecular microbiology.

[74]  H. Engelberg-Kulka,et al.  An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3',5'-bispyrophosphate: a model for programmed bacterial cell death. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  M. Inouye,et al.  Characterization of mRNA Interferases from Mycobacterium tuberculosis* , 2006, Journal of Biological Chemistry.

[76]  H. Barner,et al.  STUDIES ON UNBALANCED GROWTH IN ESCHERICHIA COLI. , 1954, Proceedings of the National Academy of Sciences of the United States of America.

[77]  J. Davies,et al.  8 Antibiotic resistance in bacteria , 1998 .

[78]  E. Ohtsubo,et al.  chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100 , 1993, Journal of bacteriology.

[79]  K. Gerdes,et al.  Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins , 2002, Molecular microbiology.

[80]  M. Yarmolinsky,et al.  Programmed cell death in bacterial populations , 1995, Science.

[81]  G. Schreiber,et al.  The nucleotide sequence and characterization of the relA gene of Escherichia coli. , 1988, The Journal of biological chemistry.

[82]  H. Engelberg-Kulka,et al.  Postsegregational Killing Mediated by the P1 Phage “Addiction Module” phd-doc Requires the Escherichia coli Programmed Cell Death SystemmazEF , 2001, Journal of bacteriology.

[83]  L. Wyns,et al.  Recognition of the Intrinsically Flexible Addiction Antidote MazE by a Dromedary Single Domain Antibody Fragment , 2003, The Journal of Biological Chemistry.

[84]  M. Swanson,et al.  Differentiate to thrive: lessons from the Legionella pneumophila life cycle , 2004, Molecular microbiology.

[85]  E. Ohtsubo,et al.  Mapping and disruption of the chpB locus in Escherichia coli , 1994, Journal of bacteriology.

[86]  B. Bassler,et al.  Quorum sensing: cell-to-cell communication in bacteria. , 2005, Annual review of cell and developmental biology.

[87]  Junying Yuan,et al.  Autophagy in cell death: an innocent convict? , 2005, The Journal of clinical investigation.

[88]  F. W. Bech,et al.  Sequence of the relB transcription unit from Escherichia coli and identification of the relB gene. , 1985, The EMBO journal.

[89]  H. Engelberg-Kulka,et al.  Addiction modules and programmed cell death and antideath in bacterial cultures. , 1999, Annual review of microbiology.

[90]  S. Bertholet,et al.  Programmed cell death in the unicellular protozoan parasite Leishmania , 2002, Cell Death and Differentiation.

[91]  H. Engelberg-Kulka,et al.  rexB of bacteriophage λ is an anti-cell death gene , 1998 .

[92]  S. Kjelleberg,et al.  Bacterial biofilms: prokaryotic adventures in multicellularity. , 2003, Current opinion in microbiology.