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Volumn 33, Issue 4, 2016, Pages 885-897

Evolutionary paths that expand plasmid host-range: Implications for spread of antibiotic resistance

Author keywords

Antibiotic resistance; Broad host range plasmid; Epistasis; Experimental evolution; Horizontal gene transfer; Pseudomonas; Resolvase; Toxin Antitoxin; Transposon

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; EPISTASIS; GENE DELETION; HOST RANGE; MOLECULAR GENETICS; PLASMID; POPULATION DYNAMICS; PSEUDOMONAS; TRANSPOSON; DNA SEQUENCE; DRUG EFFECTS; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; MOLECULAR EVOLUTION; PATHOGENICITY;

EID: 84964854840     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv339     Document Type: Article
Times cited : (90)

References (63)
  • 1
    • 84901587064 scopus 로고    scopus 로고
    • Model selection for ecologists: The worldviews of AIC and BIC
    • Aho K, Derryberry D, Peterson T. 2014. Model selection for ecologists: The worldviews of AIC and BIC. Ecology 95:631-636.
    • (2014) Ecology , vol.95 , pp. 631-636
    • Aho, K.1    Derryberry, D.2    Peterson, T.3
  • 2
    • 0023694037 scopus 로고
    • Evolution of a bacteria/plasmid association
    • Bouma JE, Lenski RE. 1988. Evolution of a bacteria/plasmid association. Nature 335:351-352.
    • (1988) Nature , vol.335 , pp. 351-352
    • Bouma, J.E.1    Lenski, R.E.2
  • 3
    • 34250108028 scopus 로고
    • Model selection and Akaike Information Criterion (AIC)- The general- Theory and its analytical extensions
    • Bozdogan H. 1987. Model selection and Akaike Information Criterion (AIC)- The general- Theory and its analytical extensions. Psychometrika 52:345-370.
    • (1987) Psychometrika , vol.52 , pp. 345-370
    • Bozdogan, H.1
  • 4
    • 78650752639 scopus 로고    scopus 로고
    • AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons
    • Burnham K, Anderson D, Huyvaert K. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 65:23-35.
    • (2011) Behav Ecol Sociobiol , vol.65 , pp. 23-35
    • Burnham, K.1    Anderson, D.2    Huyvaert, K.3
  • 6
    • 0035807805 scopus 로고    scopus 로고
    • RelE, a global inhibitor of translation, is activated during nutritional stress
    • Christensen SK, Mikkelsen M, Pedersen K, Gerdes K. 2001. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc Natl Acad Sci U S A. 98:14328-14333.
    • (2001) Proc Natl Acad Sci U S A , vol.98 , pp. 14328-14333
    • Christensen, S.K.1    Mikkelsen, M.2    Pedersen, K.3    Gerdes, K.4
  • 7
    • 0033740341 scopus 로고    scopus 로고
    • Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids
    • Cooper TF, Heinemann JA. 2000. Postsegregational killing does not increase plasmid stability but acts to mediate the exclusion of competing plasmids. Proc Natl Acad Sci U S A. 97:12643-12648.
    • (2000) Proc Natl Acad Sci U S A , vol.97 , pp. 12643-12648
    • Cooper, T.F.1    Heinemann, J.A.2
  • 8
    • 0347992016 scopus 로고    scopus 로고
    • Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12
    • Dahlberg C, Chao L. 2003. Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165:1641-1649.
    • (2003) Genetics , vol.165 , pp. 1641-1649
    • Dahlberg, C.1    Chao, L.2
  • 9
    • 0034612342 scopus 로고    scopus 로고
    • One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
    • Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 97:6640-6645.
    • (2000) Proc Natl Acad Sci U S A , vol.97 , pp. 6640-6645
    • Datsenko, K.A.1    Wanner, B.L.2
  • 10
    • 10844248054 scopus 로고    scopus 로고
    • Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution
    • De Gelder L, Ponciano JM, Abdo Z, Joyce P, Forney LJ, Top EM. 2004. Combining mathematical models and statistical methods to understand and predict the dynamics of antibiotic-sensitive mutants in a population of resistant bacteria during experimental evolution. Genetics 168:1131-1144.
    • (2004) Genetics , vol.168 , pp. 1131-1144
    • De Gelder, L.1    Ponciano, J.M.2    Abdo, Z.3    Joyce, P.4    Forney, L.J.5    Top, E.M.6
  • 11
    • 33847231339 scopus 로고    scopus 로고
    • Stability of a promiscuous plasmid in different hosts: No guarantee for a long- Term relationship
    • De Gelder L, Ponciano JM, Joyce P, Top EM. 2007. Stability of a promiscuous plasmid in different hosts: no guarantee for a long- Term relationship. Microbiology 153:452-463.
    • (2007) Microbiology , vol.153 , pp. 452-463
    • De Gelder, L.1    Ponciano, J.M.2    Joyce, P.3    Top, E.M.4
  • 12
    • 45849099491 scopus 로고    scopus 로고
    • Adaptive plasmid evolution results in host-range expansion of a broad-hostrange plasmid
    • De Gelder L, Williams JJ, Ponciano JM, Sota M, Top EM. 2008. Adaptive plasmid evolution results in host-range expansion of a broad-hostrange plasmid. Genetics 178:2179-2190.
    • (2008) Genetics , vol.178 , pp. 2179-2190
    • De Gelder, L.1    Williams, J.J.2    Ponciano, J.M.3    Sota, M.4    Top, E.M.5
  • 14
    • 25444496227 scopus 로고    scopus 로고
    • The evolution of a conjugative plasmid and its ability to increase bacterial fitness
    • Dionisio F, Conceiçao IC, Marques AC, Fernandes L, Gordo I. 2005. The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett. 1:250-252.
    • (2005) Biol Lett , vol.1 , pp. 250-252
    • Dionisio, F.1    Conceiçao, I.C.2    Marques, A.C.3    Fernandes, L.4    Gordo, I.5
  • 15
    • 0023405209 scopus 로고
    • The sequence encoding the 43-kilodalton trfA protein is required for efficient replication or maintenance of minimal RK2 replicons in Pseudomonas aeruginosa
    • Durland RH, Helinski DR. 1987. The sequence encoding the 43-kilodalton trfA protein is required for efficient replication or maintenance of minimal RK2 replicons in Pseudomonas aeruginosa. Plasmid 18:164-169.
    • (1987) Plasmid , vol.18 , pp. 164-169
    • Durland, R.H.1    Helinski, D.R.2
  • 16
    • 33947373975 scopus 로고    scopus 로고
    • The SXT conjugative element and linear prophage N15 encode toxin- Antitoxin- stabilizing systems homologous to the tad- Ata module of the Paracoccus aminophilus plasmid pAMI2
    • Dziewit L, Jazurek M, Drewniak L, Baj J, Bartosik D. 2007. The SXT conjugative element and linear prophage N15 encode toxin- Antitoxin- stabilizing systems homologous to the tad- Ata module of the Paracoccus aminophilus plasmid pAMI2. J Bacteriol. 189:1983-1997.
    • (2007) J Bacteriol , vol.189 , pp. 1983-1997
    • Dziewit, L.1    Jazurek, M.2    Drewniak, L.3    Baj, J.4    Bartosik, D.5
  • 17
    • 29444437147 scopus 로고    scopus 로고
    • Plasmid segregation mechanisms
    • Ebersbach G, Gerdes K. 2005. Plasmid segregation mechanisms. Annu Rev Genet. 39:453-479.
    • (2005) Annu Rev Genet , vol.39 , pp. 453-479
    • Ebersbach, G.1    Gerdes, K.2
  • 18
    • 0031455398 scopus 로고    scopus 로고
    • The twocomponent signaling pathway of bacterial chemotaxis: A molecular view of signal transduction by receptors, kinases, and adaptation enzymes
    • Falke JJ, Bass RB, Butler SL, Chervitz SA, Danielson MA. 1997. The twocomponent signaling pathway of bacterial chemotaxis: A molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol. 13:457-512.
    • (1997) Annu Rev Cell Dev Biol , vol.13 , pp. 457-512
    • Falke, J.J.1    Bass, R.B.2    Butler, S.L.3    Chervitz, S.A.4    Danielson, M.A.5
  • 19
    • 80053492422 scopus 로고    scopus 로고
    • Multicopy plasmid stability: Revisiting the dimer catastrophe
    • Field CM, Summers DK. 2011. Multicopy plasmid stability: Revisiting the dimer catastrophe. J Theor Biol. 291:119-127.
    • (2011) J Theor Biol , vol.291 , pp. 119-127
    • Field, C.M.1    Summers, D.K.2
  • 21
    • 0021992145 scopus 로고
    • Stable inheritance of plasmid R1 requires two different loci
    • Gerdes K, Larsen JE, Molin S. 1985. Stable inheritance of plasmid R1 requires two different loci. J Bacteriol. 161:292-298.
    • (1985) J Bacteriol , vol.161 , pp. 292-298
    • Gerdes, K.1    Larsen, J.E.2    Molin, S.3
  • 22
    • 0345333119 scopus 로고
    • Unique type of plasmid maintenance function: Postsegregational killing of plasmid-free cells
    • Gerdes K, Rasmussen PB, Molin S. 1986. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci U S A. 83:3116-3120.
    • (1986) Proc Natl Acad Sci U S A , vol.83 , pp. 3116-3120
    • Gerdes, K.1    Rasmussen, P.B.2    Molin, S.3
  • 23
    • 84892892483 scopus 로고    scopus 로고
    • Toxin- Antitoxin systems as multilevel interaction systems
    • Basel
    • Goeders N, Van Melderen L. 2014. Toxin- Antitoxin systems as multilevel interaction systems. Toxins (Basel) 6:304-324.
    • (2014) Toxins , vol.6 , pp. 304-324
    • Goeders, N.1    Van Melderen, L.2
  • 24
    • 84907855211 scopus 로고    scopus 로고
    • Phenotypic Interactions amongmutations in a Thermus thermophilus 16S rRNA gene detected with genetic selections and experimental evolution
    • Gregory ST, Connetti JL, Carr JF, Jogl G, Dahlberg AE. 2014. Phenotypic Interactions amongmutations in a Thermus thermophilus 16S rRNA gene detected with genetic selections and experimental evolution. J Bacteriol 196:3776-3783.
    • (2014) J Bacteriol , vol.196 , pp. 3776-3783
    • Gregory, S.T.1    Connetti, J.L.2    Carr, J.F.3    Jogl, G.4    Dahlberg, A.E.5
  • 25
    • 85158006363 scopus 로고    scopus 로고
    • The movement of Tn3-like elements: Transposition and cointegrate resolution
    • Craig N, Craigie R, Gellert M, Lambowitz A, editors. (DC): ASM Press
    • Grindley NDF. 2002. The movement of Tn3-like elements: Transposition and cointegrate resolution. In: Craig N, Craigie R, Gellert M, Lambowitz A, editors. Mobile DNA II. Washington (DC): ASM Press. p. 272-302.
    • (2002) Mobile DNA II. Washington , pp. 272-302
    • Grindley, N.D.F.1
  • 26
    • 0020959710 scopus 로고
    • Studies on transformation of Escherichia coli with plasmids
    • Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 166:557-580.
    • (1983) J Mol Biol , vol.166 , pp. 557-580
    • Hanahan, D.1
  • 27
    • 84938751775 scopus 로고    scopus 로고
    • Parallel compensatory evolution stabilizes plasmids across the parasitism- mutualism continuum
    • Harrison E, Guymer D, Spiers AJ, Paterson S, Brockhurst MA. 2015. Parallel compensatory evolution stabilizes plasmids across the parasitism- mutualism continuum. Curr Biol. 25(15): 2034-2039.
    • (2015) Curr Biol , vol.25 , Issue.15 , pp. 2034-2039
    • Harrison, E.1    Guymer, D.2    Spiers, A.J.3    Paterson, S.4    Brockhurst, M.A.5
  • 28
    • 0141707105 scopus 로고    scopus 로고
    • Toxins- Antitoxins: Plasmid maintenance, programmed cell death, and cell cycle arrest
    • Hayes F. 2003. Toxins- Antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301:1496-1499.
    • (2003) Science , vol.301 , pp. 1496-1499
    • Hayes, F.1
  • 29
    • 33847234930 scopus 로고    scopus 로고
    • Frequent conjugative transfer accelerates adaptation of a broad-host-range plasmid to an unfavorable Pseudomonas putida host
    • Heuer H, Fox RE, Top EM. 2007. Frequent conjugative transfer accelerates adaptation of a broad-host-range plasmid to an unfavorable Pseudomonas putida host. FEMS Microbiol Ecol. 59:738-748.
    • (2007) FEMS Microbiol Ecol , vol.59 , pp. 738-748
    • Heuer, H.1    Fox, R.E.2    Top, E.M.3
  • 32
    • 21244475684 scopus 로고    scopus 로고
    • Modeling the impact of periodic bottlenecks, unidirectional mutation, and observational error in experimental evolution
    • Joyce P, Abdo Z, Ponciano JM, De Gelder L, Forney LJ, Top EM. 2005. Modeling the impact of periodic bottlenecks, unidirectional mutation, and observational error in experimental evolution. J Math Biol. 50:645-662.
    • (2005) J Math Biol , vol.50 , pp. 645-662
    • Joyce, P.1    Abdo, Z.2    Ponciano, J.M.3    De Gelder, L.4    Forney, L.J.5    Top, E.M.6
  • 33
    • 84874059707 scopus 로고    scopus 로고
    • Entering a post- Antibiotic era?
    • Kahrstrom CT. 2013. Entering a post- Antibiotic era? Nat Rev Microbiol. 11:146.
    • (2013) Nat Rev Microbiol , vol.11 , pp. 146
    • Kahrstrom, C.T.1
  • 34
    • 33846011830 scopus 로고    scopus 로고
    • Plasmid pBP136 from Bordetella pertussis represents an ancestral form of IncP-1beta plasmids without accessory mobile elements
    • Kamachi K, Sota M, Tamai Y, Nagata N, Konda T, Inoue T, Top M, Arakawa Y. 2006. Plasmid pBP136 from Bordetella pertussis represents an ancestral form of IncP-1beta plasmids without accessory mobile elements. Microbiology 152:3477-3484.
    • (2006) Microbiology , vol.152 , pp. 3477-3484
    • Kamachi, K.1    Sota, M.2    Tamai, Y.3    Nagata, N.4    Konda, T.5    Inoue, T.6    Top, M.7    Arakawa, Y.8
  • 35
    • 84923205126 scopus 로고    scopus 로고
    • Coupling between the basic replicon and the Kis-Kid maintenance system of plasmid R1: Modulation by Kis antitoxin levels and involvement in control of plasmid replication
    • Lopez-Villarejo J, Lobato-Marquez D, Diaz-Orejas R. 2015. Coupling between the basic replicon and the Kis-Kid maintenance system of plasmid R1: modulation by Kis antitoxin levels and involvement in control of plasmid replication. Toxins 7:478-492.
    • (2015) Toxins , vol.7 , pp. 478-492
    • Lopez-Villarejo, J.1    Lobato-Marquez, D.2    Diaz-Orejas, R.3
  • 36
    • 67650744255 scopus 로고    scopus 로고
    • The effect of the location of the proteic post-segregational stability system within the replicon of plasmid pTF-FC2 on the fine regulation of plasmid replication
    • Matcher GF, Rawlings DE. 2009. The effect of the location of the proteic post-segregational stability system within the replicon of plasmid pTF-FC2 on the fine regulation of plasmid replication. Plasmid 62:98-107.
    • (2009) Plasmid , vol.62 , pp. 98-107
    • Matcher, G.F.1    Rawlings, D.E.2
  • 37
  • 38
    • 0026049049 scopus 로고
    • Coevolution in bacterial-plasmid populations
    • Modi RI, Adams J. 1991. Coevolution in bacterial-plasmid populations. Evolution 45:656-667.
    • (1991) Evolution , vol.45 , pp. 656-667
    • Modi, R.I.1    Adams, J.2
  • 39
    • 0026280941 scopus 로고
    • Plasmid macroevolution: Selection of deletions during adaptation in a nutrientlimited environment
    • Modi RI, Wilke CM, Rosenzweig RF, Adams J. 1991. Plasmid macroevolution: selection of deletions during adaptation in a nutrientlimited environment. Genetica 84:195-202.
    • (1991) Genetica , vol.84 , pp. 195-202
    • Modi, R.I.1    Wilke, C.M.2    Rosenzweig, R.F.3    Adams, J.4
  • 40
    • 0001615484 scopus 로고
    • Theoretical implications for the evolution of postsegregational killing by bacterial plasmids
    • Mongold JA. 1992. Theoretical implications for the evolution of postsegregational killing by bacterial plasmids. Am Nat. 139:689-677.
    • (1992) Am Nat , vol.139 , pp. 677-689
    • Mongold, J.A.1
  • 42
    • 33847188754 scopus 로고    scopus 로고
    • The population biology of bacterial plasmids: A hidden Markov model approach
    • Ponciano JM, De Gelder L, Top EM, Joyce P. 2007. The population biology of bacterial plasmids: A hidden Markov model approach. Genetics 176:957-968.
    • (2007) Genetics , vol.176 , pp. 957-968
    • Ponciano, J.M.1    De Gelder, L.2    Top, E.M.3    Joyce, P.4
  • 43
    • 78650305634 scopus 로고    scopus 로고
    • What traits are carried on mobile genetic elements, and why?
    • Edinb
    • Rankin DJ, Rocha EP, Brown SP. 2011. What traits are carried on mobile genetic elements, and why? Heredity (Edinb) 106:1-10.
    • (2011) Heredity , vol.106 , pp. 1-10
    • Rankin, D.J.1    Rocha, E.P.2    Brown, S.P.3
  • 44
    • 0001201909 scopus 로고
    • Bayesian model selection in social research
    • Raftery AE. 1995. Bayesian model selection in social research. Sociol Methodol. 25:111-163.
    • (1995) Sociol Methodol , vol.25 , pp. 111-163
    • Raftery, A.E.1
  • 47
    • 84894324351 scopus 로고    scopus 로고
    • Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations
    • San Millan A, Heilbron K, Maclean RC. 2014. Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations. ISME J. 8:601-612.
    • (2014) ISME J , vol.8 , pp. 601-612
    • San, M.A.1    Heilbron, K.2    Maclean, R.C.3
  • 49
    • 84928402541 scopus 로고    scopus 로고
    • Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa
    • San Millan A, Toll-Riera M, Qi Q, MacLean RC. 2015. Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa. Nat Commun. 6:6845.
    • (2015) Nat Commun , vol.6 , pp. 6845
    • San, M.A.1    Toll-Riera, M.2    Qi, Q.3    MacLean, R.C.4
  • 52
    • 34548638261 scopus 로고    scopus 로고
    • Structure and mechanism of helicases and nucleic acid translocases
    • Singleton MR, Dillingham MS, Wigley DB. 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem. 76:23-50.
    • (2007) Annu Rev Biochem , vol.76 , pp. 23-50
    • Singleton, M.R.1    Dillingham, M.S.2    Wigley, D.B.3
  • 53
    • 78649446843 scopus 로고    scopus 로고
    • Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein
    • Sota M, Yano H, Julie HM, Daughdrill GW, Abdo Z, Forney Z, Top EM. 2010. Shifts in the host range of a promiscuous plasmid through parallel evolution of its replication initiation protein. ISME J 4:1568-1580.
    • (2010) ISME J , vol.4 , pp. 1568-1580
    • Sota, M.1    Yano, H.2    Julie, H.M.3    Daughdrill, G.W.4    Abdo, Z.5    Forney, Z.6    Top, E.M.7
  • 55
    • 0031690672 scopus 로고    scopus 로고
    • Efficiency of the pTF-FC2 pas poisonantidote stability system in Escherichia coli is affected by the host strain, and antidote degradation requires the Lon Protease
    • Smith ASG, Rawlings DE. 1998. Efficiency of the pTF-FC2 pas poisonantidote stability system in Escherichia coli is affected by the host strain, and antidote degradation requires the Lon Protease. J Bacteriol. 180:5458-5462.
    • (1998) J Bacteriol , vol.180 , pp. 5458-5462
    • Smith, A.S.G.1    Rawlings, D.E.2
  • 56
    • 0017652638 scopus 로고
    • The population biology of bacterial plasmids: A priori conditions for the existence of conjugationally transmitted factors
    • Stewart FM, Levin BR. 1977. The population biology of bacterial plasmids: A priori conditions for the existence of conjugationally transmitted factors. Genetics 87:209-228.
    • (1977) Genetics , vol.87 , pp. 209-228
    • Stewart, F.M.1    Levin, B.R.2
  • 58
    • 84953635804 scopus 로고    scopus 로고
    • Evidential statistics as a statistical modern synthesis to support 21st century science
    • Taper ML, Ponciano JM. 2016. Evidential statistics as a statistical modern synthesis to support 21st century science. Popu Ecol. 58:9-29.
    • (2016) Popu Ecol , vol.58 , pp. 9-29
    • Taper, M.L.1    Ponciano, J.M.2
  • 59
    • 46249089476 scopus 로고    scopus 로고
    • Model structure adequacy analysis: Selecting models on the basis of their ability to answer scientific questions
    • Taper ML, Staples DF, Shepard BB. 2008. Model structure adequacy analysis: selecting models on the basis of their ability to answer scientific questions. Synthese 163:357-370.
    • (2008) Synthese , vol.163 , pp. 357-370
    • Taper, M.L.1    Staples, D.F.2    Shepard, B.B.3
  • 60
    • 0031922777 scopus 로고    scopus 로고
    • Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids
    • Turner PE, Cooper SV, Lenski RE. 1998. Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52:315-329.
    • (1998) Evolution , vol.52 , pp. 315-329
    • Turner, P.E.1    Cooper, S.V.2    Lenski, R.E.3
  • 61
    • 84901809320 scopus 로고    scopus 로고
    • World Health Organization. Geneva: WHO Press. Available from
    • World Health Organization. 2014. Antimicrobial resistance: global report on surveillance 2014. Geneva: WHO Press. Available from: http://apps.who.int/iris/handle/10665/112642.
    • (2014) Antimicrobial Resistance: Global Report on Surveillance 2014
  • 62
    • 77956548642 scopus 로고    scopus 로고
    • Complete nucleotide sequence of TOL plasmid pDK1 provides evidence for evolutionary history of IncP-7 catabolic plasmids
    • Yano H, Miyakoshi M, Ohshima K, Tabata M, Nagata Y, Hattori M, Tsuda M. 2010. Complete nucleotide sequence of TOL plasmid pDK1 provides evidence for evolutionary history of IncP-7 catabolic plasmids. J Bacteriol. 192:4337-4347.
    • (2010) J Bacteriol , vol.192 , pp. 4337-4347
    • Yano, H.1    Miyakoshi, M.2    Ohshima, K.3    Tabata, M.4    Nagata, Y.5    Hattori, M.6    Tsuda, M.7
  • 63
    • 0028963606 scopus 로고
    • Programmed cell death in bacterial populations
    • Yarmolinsky MB. 1995. Programmed cell death in bacterial populations. Science 267:836-837.
    • (1995) Science , vol.267 , pp. 836-837
    • Yarmolinsky, M.B.1


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