Bacterial autolysis has recently been identified as a key mechanism that regulates different phases of biofilm development including microcolony formation and dispersal. However such autolytic measures are limited to a subfraction of cells within the entire biofilm population. Here we speculate on the role biofilm heterogeneity plays in limiting autolysis within biofilms and further describe the molecular regulation of suicidal and fratricidal mechanisms in biofilm development of Staphylococcus aureus and Enterococcus faecalis.
RobertsR.C., MohrC.D., ShapiroL.. Developmental programs in bacteria.Curr Top Dev Biol1996; 34: 207–57.
2.
DriksA.. Overview: Development in bacteria: spore formation in Bacillus subtilis.Cell Mol Life Sci2002; 59: 389–91.
3.
ClaverysJ.P., HavarsteinL.S.. Cannibalism and fratricide: mechanisms and raisons d'etre.Nat Rev Microbiol2007; 5: 219–29.
4.
Hall-StoodleyL., CostertonJ.W., StoodleyP.. Bacterial biofilms: from the natural environment to infectious diseases.Nat Rev Microbiol2004; 2: 95–108.
5.
CostertonJ.W., StewartP.S., GreenbergE.P.. Bacterial biofilms: a common cause of persistent infections.Science1999; 284: 1318–22.
6.
HoyleB.D., CostertonJ.W.. Bacterial resistance to antibiotics: the role of biofilms.Prog Drug Res1991; 37: 91–105.
7.
CostertonJ.W., MontanaroL., ArciolaC.R.. Biofilm in implant infections: its production and regulation.Int J Artif Organs2005; 28: 1062–8.
8.
GilbertP., AllisonD.G., McBainA.J.. Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance?Symp Ser Soc Appl Microbiol2002: S98–110.
9.
RiceK.C., BaylesK.W.. Molecular control of bacterial death and lysis.Microbiol Mol Biol Rev2008; 72: 85–109.
10.
BaylesK.W.. The biological role of death and lysis in biofilm development.Nat Rev Microbiol2007; 5: 721–6.
11.
NadellC.D., XavierJ.B., FosterK.R.. The sociobiology of biofilms.FEMS Microbiol Rev2009; 33: 206–24.
TetzG.V., ArtemenkoN.K., TetzV.V.. Effect of DNase and antibiotics on biofilm characteristics.Antimicrob Agents Chemother2009; 53: 1204–9.
16.
VilainS., PretoriusJ.M., TheronJ., BrozelV.S.. DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms.Appl Environ Microbiol2009; 75: 2861–8.
17.
WhitchurchC.B., Tolker-NielsenT., RagasP.C., MattickJ.S.. Extracellular DNA required for bacterial biofilm formation.Science2002; 295: 1487.
18.
ThomasV.C., ThurlowL.R., BoyleD., HancockL.E.. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development.J Bacteriol2008; 190: 5690–8.
19.
Allesen-HolmM., BarkenK.B., YangL., KlausenM., WebbJ.S., KjellebergS.. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms.Mol Microbiol2006; 59: 1114–28.
20.
MulcahyH., Charron-MazenodL., LewenzaS.. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms.PLoS Pathog2008; 4: e1000213.
21.
Mai-ProchnowA., EvansF., Dalisay-SaludesD., StelzerS., EganS., JamesS.. Biofilm development and cell death in the marine bacterium Pseudoalteromonas tunicata.Appl Environ Microbiol2004; 70: 3232–8.
22.
WebbJ.S., ThompsonL.S., JamesS., CharltonT., Tolker-NielsenT., KochB.. Cell death in Pseudomonas aeruginosa biofilm development.J Bacteriol2003; 185: 4585–92.
23.
Mai-ProchnowA., WebbJ.S., FerrariB.C., KjellebergS.. Eco-logical advantages of autolysis during the development and dispersal of Pseudoalteromonas tunicata biofilms.Appl Environ Microbiol2006; 72: 5414–20.
24.
StewartP.S., FranklinM.J.. Physiological heterogeneity in biofilms.Nat Rev Microbiol2008; 6: 199–210.
25.
ElowitzM.B., LevineA.J., SiggiaE.D., SwainP.S.. Stochastic gene expression in a single cell.Science2002; 297: 1183–6.
26.
SwainP.S., ElowitzM.B., SiggiaE.D.. Intrinsic and extrinsic contributions to stochasticity in gene expression.Proc Natl Acad Sci U S A2002; 99: 12795–800.
VeeningJ.W., SmitsW.K., KuipersO.P.. Bistability, epigenetics, and bet-hedging in bacteria.Annu Rev Microbiol2008; 62: 193–210.
29.
VeeningJ.W., StewartE.J., BerngruberT.W., TaddeiF., KuipersO.P., HamoenL.W.. Bet-hedging and epigenetic inheritance in bacterial cell development.Proc Natl Acad Sci U S A2008; 105: 4393–8.
30.
DavidsonC.J., SuretteM.G.. Individuality in bacteria.Annu Rev Genet2008; 42: 253–68.
31.
KjellebergS., MolinS.. Is there a role for quorum sensing signals in bacterial biofilms?Curr Opin Microbiol2002; 5: 254–8.
32.
DubnauD., LosickR.. Bistability in bacteria.Mol Microbiol2006; 61: 564–72.
33.
SauerK., CamperA.K.. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth.J Bacteriol2001; 183: 6579–89.
LeeJ., JayaramanA., WoodT.K.. Indole is an inter-species biofilm signal mediated by SdiA.BMC Microbiol2007; 7: 42.
36.
IrieY., ParsekM.R.. Quorum sensing and microbial biofilms.Curr Top Microbiol Immunol2008; 322: 67–84.
37.
ProutyA.M., SchwesingerW.H., GunnJ.S.. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp.Infect Immun2002; 70: 2640–9.
38.
ColeS.P., HarwoodJ., LeeR., SheR., GuineyD.G.. Characterization of monospecies biofilm formation by Helicobacter pylori.J Bacteriol2004; 186: 3124–32.
39.
MoyedH.S., BertrandK.P.. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis.J Bacteriol1983; 155: 768–75.
40.
DriffieldK., MillerK., BostockJ.M., O'NeillA.J., ChopraI.. Increased mutability of Pseudomonas aeruginosa in biofilms.J Antimicrob Chemother2008; 61: 1053–6.
41.
OliverA., BaqueroF., BlazquezJ.. The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants.Mol Microbiol2002; 43: 1641–50.
42.
ChopraI., O'NeillA.J., MillerK.. The role of mutators in the emergence of antibiotic-resistant bacteria.Drug Resist Updat2003; 6: 137–45.
43.
ChiaN., WoeseC.R., GoldenfeldN.. A collective mechanism for phase variation in biofilms.Proc Natl Acad Sci U S A2008; 105: 14597–602.
44.
KiemS., OhW.S., PeckK.R.. Phase variation of biofilm formation in Staphylococcus aureus by IS 256 insertion and its impact on the capacity adhering to polyurethane surface.J Korean Med Sci2004; 19: 779–82.
45.
TormoM.A., UbedaC., MartiM.. Phase-variable expression of the biofilm-associated protein (Bap) in Staphylococcus aureus.Microbiology2007; 153: 1702–10.
46.
ConlonK.M., HumphreysH., O'GaraJ.P.. Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis.J Bacteriol2004; 186: 6208–19.
47.
MaL., ConoverM., LuH., ParsekM.R., BaylesK., WozniakD.J.. Assembly and development of the Pseudomonas aeruginosa biofilm matrix.PLoS Pathog2009; 5: e1000354.
48.
EllermeierC.D., HobbsE.C., Gonzalez-PastorJ.E., LosickR.. A three-protein signaling pathway governing immunity to a bacterial cannibalism toxin.Cell2006; 124: 549–59.
49.
BurbulysD., TrachK.A., HochJ.A.. Initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay.Cell1991; 64: 545–52.
50.
ChungJ.D., StephanopoulosG., IretonK., GrossmanA.D.. Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation.J Bacteriol1994; 176: 1977–84.
51.
Gonzalez-PastorJ.E., HobbsE.C., LosickR.. Cannibalism by sporulating bacteria.Science2003; 301: 510–3.
52.
WeiserJ.N., MarkiewiczZ., TuomanenEl, WaniJ.H.. Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae.Infect Immun1996; 64: 2240–5.
53.
ThomasV.C., HiromasaY., HarmsN., ThurlowL., TomichJ., HancockL.E.. A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis.Mol Microbiol2009; 72: 1022–36.
54.
LewisK.. Programmed death in bacteria.Microbiol Mol Biol Rev2000; 64: 503–14.
55.
RiceK.C., MannE.E., EndresJ.L., WeissE.C., CassatJ.E., SmeltzerM.S.. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus.Proc Natl Acad Sci U S A2007; 104: 8113–8.
56.
HettsS.W.. To die or not to die: an overview of apoptosis and its role in disease.JAMA1998; 279: 300–7.
57.
ShockmanG.D., Daneo-MooreL., KariyamaR., MassiddaO.. Bacterial walls, peptidoglycan hydrolases, autolysins, and autolysis.Microb Drug Resist1996; 2: 95–8.
58.
BrunskillE.W., BaylesK.W.. Identification of LytSR-regulated genes from Staphylococcus aureus.J Bacteriol1996; 178: 5810–2.
59.
WangI.N., SmithD.L., YoungR.. Holins: the protein clocks of bacteriophage infections.Annu Rev Microbiol2000; 54: 799–825.
60.
GrundlingA., MansonM.D., YoungR.. Holins kill without warning.Proc Natl Acad Sci U S A2001; 98: 9348–52.
61.
RiceK.C., FirekB.A., NelsonJ.B., YangS.J., PattonT.G., BaylesK.W.. The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance.J Bacteriol2003; 185: 2635–43.
62.
PattonT.G., RiceK.C., FosterM.K., BaylesK.W.. The Staphylococcus aureus cidC gene encodes a pyruvate oxidase that affects acetate metabolism and cell death in stationary phase.Mol Microbiol2005; 56: 1664–74.
63.
RiceK.C., NelsonJ.B., PattonT.G., YangS.J., BaylesK.W.. Ace-tic acid induces expression of the Staphylococcus aureus cidABC and IrgAB murein hydrolase regulator operons.J Bacteriol2005; 187: 813–21.
64.
PattonT.G., YangS.J., BaylesK.W.. The role of proton motive force in expression of the Staphylococcus aureus cid and Irg operons.Mol Microbiol2006; 59: 1395–404.
65.
GroicherK.H., FirekB.A., FujimotoD.F., BaylesK.W.. The Staphylococcus aureus IrgAB operon modulates murein hydrolase activity and penicillin tolerance.J Bacteriol2000; 182: 1794–801.
66.
StewartP.S.. Diffusion in biofilms.J Bacteriol2003; 185: 1485–91.
67.
YangS.J., RiceK.C., BrownR.J., PattonT.G., LiouL.E., ParkY.H.. A LysR-type regulator, CidR, is required for induction of the Staphylococcus aureus cidABC operon.J Bacteriol2005; 187: 5893–900.
68.
YangS.J., DunmanP.M., ProjanS.J., BaylesK.W.. Characterization of the Staphylococcus aureus CidR regulon: elucidation of a novel role for acetoin metabolism in cell death and lysis.Mol Microbiol2006; 60: 458–68.
69.
HancockL.E., PeregoM.. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase.J Bacteriol2004; 186: 5629–39.
70.
QinX., SinghK.V., WeinstockG.M., MurrayB.E.. Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF.J Bacteriol2001; 183: 3372–82.
71.
NishiguchiK., NagataK., TanokuraM., SonomotoK., NakayamaJ.. Structure-activity relationship of gelatinase biosynthesis-activating pheromone of Enterococcus faecalis.J Bacteriol2009; 191: 641–50.
72.
NakayamaJ., ChenS., OyamaN.. Revised model for Enterococcus faecalis fsr quorum-sensing system: the small open reading frame fsrD encodes the gelatinase biosynthesis-activating pheromone propeptide corresponding to staphylococcal agrD.J Bacteriol2006; 188: 8321–6.
73.
NakayamaJ., CaoY., HoriiT.. Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis.Mol Microbiol2001; 41: 145–54.
74.
QinX., SinghK.V., WeinstockG.M., MurrayB.E.. Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence.Infect Immun2000; 68: 2579–86.
75.
BourgogneA., HilsenbeckS.G., DunnyG.M., MurrayB.E.. Comparison of OG1RF and an isogenic fsrB deletion mutant by transcriptional analysis: the Fsr system of Enterococcus faecalis is more than the activator of gelatinase and serine protease.J Bacteriol2006; 188: 2875–84.
