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

Leen De Gelder UGent, José Ponciano, Paul Joyce and Eva Top (2007) MICROBIOLOGY-SGM. 153(2). p.452-463
abstract
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-1 beta 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
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
HORIZONTAL GENE-TRANSFER, COMPLETE GENOME SEQUENCE, ESCHERICHIA-COLI, PSEUDOMONAS-AERUGINOSA, EXPERIMENTAL EVOLUTION, BACTERIAL PLASMIDS, ACTIVATED-SLUDGE, ANTIBIOTIC-RESISTANCE, KFRA GENE, R-FACTOR
journal title
MICROBIOLOGY-SGM
Microbiology-SGM
volume
153
issue
2
pages
452 - 463
Web of Science type
Article
Web of Science id
000244422700017
JCR category
MICROBIOLOGY
JCR impact factor
3.11 (2007)
JCR rank
23/91 (2007)
JCR quartile
1 (2007)
ISSN
1350-0872
DOI
10.1099/mic.0.2006/001784-0
language
English
UGent publication?
no
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
765518
handle
http://hdl.handle.net/1854/LU-765518
date created
2009-10-19 16:44:46
date last changed
2016-12-19 15:44:30
@article{765518,
  abstract     = {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-1 beta 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},
  author       = {De Gelder, Leen and Ponciano, Jos{\'e} and Joyce, Paul and Top, Eva},
  issn         = {1350-0872},
  journal      = {MICROBIOLOGY-SGM},
  keyword      = {HORIZONTAL GENE-TRANSFER,COMPLETE GENOME SEQUENCE,ESCHERICHIA-COLI,PSEUDOMONAS-AERUGINOSA,EXPERIMENTAL EVOLUTION,BACTERIAL PLASMIDS,ACTIVATED-SLUDGE,ANTIBIOTIC-RESISTANCE,KFRA GENE,R-FACTOR},
  language     = {eng},
  number       = {2},
  pages        = {452--463},
  title        = {Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship},
  url          = {http://dx.doi.org/10.1099/mic.0.2006/001784-0},
  volume       = {153},
  year         = {2007},
}

Chicago
De Gelder, Leen, José Ponciano, Paul Joyce, and Eva Top. 2007. “Stability of a Promiscuous Plasmid in Different Hosts: No Guarantee for a Long-term Relationship.” Microbiology-sgm 153 (2): 452–463.
APA
De Gelder, L., Ponciano, J., Joyce, P., & Top, E. (2007). Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. MICROBIOLOGY-SGM, 153(2), 452–463.
Vancouver
1.
De Gelder L, Ponciano J, Joyce P, Top E. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. MICROBIOLOGY-SGM. 2007;153(2):452–63.
MLA
De Gelder, Leen, José Ponciano, Paul Joyce, et al. “Stability of a Promiscuous Plasmid in Different Hosts: No Guarantee for a Long-term Relationship.” MICROBIOLOGY-SGM 153.2 (2007): 452–463. Print.