The Maintenance of Plasmid-containing Organisms in Populations of Escherichia coli

Helling, Robert B.; Kinney, Thomas R.; Adams, Julian

doi:10.1099/00221287-123-1-129

Cited by 104 publications

(80 citation statements)

References 23 publications

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“…2) . It was proposed that they were caused by mutations in the chromosome that were beneficial independently of the plasmid (Helling et al, 1981). The fluctuations in the fraction of plasmid-free cells observed in our experiment are much smaller and mostly followed a general decrease in the plasmid-containing fraction.…”

mentioning

confidence: 55%

“…2) was much higher than what was expected from variability due to sampling alone. Highly fluctuating frequencies of plasmid-containing cells over very short time spans have been documented before (Helling et al, 1981;. It was proposed that they were caused by mutations in the chromosome that were beneficial independently of the plasmid (Helling et al, 1981).…”

Section: Mechanisms Responsible For Overall Plasmid Stabilitymentioning

confidence: 99%

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Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship

et al. 2007

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Broad-host-range (BHR) IncP-1 plasmids have the ability to transfer between and replicate in nearly all species of the Alpha-, Beta-and Gammaproteobacteria, but surprisingly few data are available on the stability of these plasmids in strains within their host range. Moreover, even though molecular interactions between the bacterial host and its plasmid(s) exist, no systematic study to date has compared the stability of the same plasmid among different hosts. The goal of this study was to examine whether the stability characteristics of an IncP-1 plasmid can be variable between strains within the host range of the plasmid. Therefore, 19 strains within the Alpha-, Beta-or Gammaproteobacteria carrying the IncP-1b plasmid pB10 were serially propagated in non-selective medium and the fraction of segregants was monitored through replica-picking. Remarkably, a large variation in the stability of pB10 in different strains was found, even between strains within the same genus or species. Ten strains showed no detectable plasmid loss over about 200 generations, and in two strains plasmid-free clones were only sporadically observed. In contrast, three strains, Pseudomonas koreensis R28, Pseudomonas putida H2 and Stenotrophomonas maltophilia P21, exhibited rapid plasmid loss within 80 generations. Parameter estimation after mathematical modelling of these stability data suggested high frequencies of segregation (about 0.04 per generation) or high plasmid cost (i.e. a relative fitness decrease in plasmid-bearing cells of about 15 and 40 %), which was confirmed experimentally. The models also suggested that plasmid reuptake by conjugation only played a significant role in plasmid stability in one of the three strains. Four of the 19 strains lost the plasmid very slowly over about 600 generations. The erratic decrease of the plasmid-containing fraction and simulation of the data with a new mathematical model suggested that plasmid cost was variable over time due to compensatory mutations. The findings of this study demonstrate that the ability of a so-called 'BHR' plasmid to persist in a bacterial population is influenced by strain-specific traits, and therefore observations made for one strain should not be generalized for the entire species or genus. INTRODUCTIONComparative analyses of fully sequenced bacterial genomes suggest that horizontal gene transfer has played a significant role in the adaptive evolution of microbial life (Gogarten & Townsend, 2005;Gogarten et al., 2002;Jain et al., 2002). In particular, horizontal transfer (HT) of broad-host-range (BHR) antibiotic resistance plasmids through conjugation is important to the spread of drug resistance genes (de la Cruz & Davies, 2000;Frost et al., 2005;Mazel & Davies, 1999), as these plasmids can transfer between and replicate in a broad range of taxonomically diverse species. Besides conjugation and replication, stability in the absence of selection for plasmid-encoded traits is a third characteristic that should be considered in the assessment of the long-term host r...

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mentioning

confidence: 55%

Section: Mechanisms Responsible For Overall Plasmid Stabilitymentioning

confidence: 99%

Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship

et al. 2007

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“…At the same time, maintenance of the plasmid and the expression of the genes (some of which may interfere with organismic processes) are costs associated with the presence of plasmids (109,137). A balance of these effects has been measured in E. coli with small, nonconjugative plasmids (viz., pACYC184 and other ColEl derivatives) in both serial (34) and continuous (137) cultures.…”

Section: Effective Abundance Of Gene Copiesmentioning

confidence: 99%

Organization of the Bacterial Chromosome

Schumann

2006

Dynamics of the Bacterial Chromosome

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“…plasmid-host relationships which are new and in which no history of association between the plasmid and the host exists (Adams et al 1979 ;Helling et al 1981 ;Noack et al 1981 ;Hartl et al 1983 ;Seo et al 1985 ;Nguyen et al 1989). It has been demonstrated, however, that a longterm history of association between plasmids and their hosts may result in beneficial coevolutionary changes in both the plasmid and the host (Bouma & Lenski 1988 ;Lenski et al 1994).…”

Section: (A) Cost Of Bacteriocin Productionmentioning

confidence: 99%

“…This feature will clearly affect the fitness of the population to some degree, but due to the small numbers of individuals involved, the relative costs should not be large due to benefits gained from killing a portion of the competing bacteria. In addition, all cells in the population will also pay a cost associated with bacteriocin plasmid carriage and replication (Adams et al 1979 ;Helling et al 1981 ;Noack et al 1981 ;Hartl et al 1983 ;Seo et al 1985 ;Nguyen et al 1989). Specifically, the expression of immunity and other plasmid-encoded proteins which assure the survival of these strains in the presence of bacteriocins will impose a cost on the population which will be expressed as a lowered maximum specific growth rate (Adams et al 1979 ;Frank 1994).…”

Section: Theoretical Backgroundmentioning

confidence: 99%

Selection and fitness in bacteriocin–producing bacteria

Dykes

Hastings

1997

Proc. R. Soc. Lond. B

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SUMMARYBacteriocins are proteinaceous anticompetitor molecules produced by bacteria against closely related species. A number of theoretical models have been used to explain experimental data that indicate high polymorphisms among bacteriocins and a frequency-dependent nature of selection for bacteriocinproducing strains. The majority of these experimental data were, however, obtained from investigations into the colicin group of bacteriocins produced by Gram-negative bacteria. The conclusions drawn from these models have been extrapolated to other bacteriocins and allelopathic compounds in general. Examination of more recent experimental investigations into the bacteriocins of Gram-positive bacteria indicate a lower degree of polymorphism and a less frequency-dependent mode of selection among these strains than among the colicin-producing strains. Here we examine these contradictions in the light of the assumptions and conclusions of the theoretical models and reported data. We show that fitness costs (as indicated by decreased relative maximum growth rate) associated with bacteriocin production may be much lower in many cases than is assumed in the present models. A lower fitness cost associated with bacteriocin production adequately explains the newer data from Gram-positive bacteria cited here, and indicates that extrapolation of existing models to all bacteriocins and other allelopathic compounds is not appropriate.

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The Maintenance of Plasmid-containing Organisms in Populations of Escherichia coli

Cited by 104 publications

References 23 publications

Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship

Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship

Organization of the Bacterial Chromosome

Selection and fitness in bacteriocin–producing bacteria

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