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Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid

Leen De Gelder UGent, Julia J Williams, José M Ponciano, Masahiro Sota and Eva M Top (2008) GENETICS. 178(4). p.2179-2190
abstract
Little is known about the range of hosts in which broad-host-range (BHR) plasmids can persist in the absence of selection for plasmid-encoded traits, and whether this "long-term host range" can evolve over time. Previously, the BHR multidrug resistance plasmid pB10 was shown to be highly unstable in Stenotrophomonas maltophilia P21 and Pseudomonas putida H2. To investigate whether this plasmid can adapt to such unfavorable hosts, we performed evolution experiments wherein pB10 was maintained in strain P21, strain H2, and alternatingly in P21 and H2. Plasmids that evolved in P21 and in both hosts showed increased stability and decreased cost in ancestral host P21. However, the latter group showed higher variability in stability patterns, suggesting that regular switching between distinct hosts hampered adaptive plasmid evolution. The plasmids evolved in P21 were also equally or more stable in other hosts compared to pB10, which suggested true host-range expansion. The complete genome sequences of four evolved plasmids with improved stability showed only one or two genetic changes. The stability of plasmids evolved in H2 improved only in their coevolved hosts, not in the ancestral host. Thus a BHR plasmid can adapt to an unfavorable host and thereby expand its long-term host range.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
PB10, SELECTION, POPULATION, HORIZONTAL GENE-TRANSFER, GRAM-NEGATIVE BACTERIA, RESISTANCE PLASMIDS, ACTIVATED-SLUDGE, BENEFICIAL MUTATIONS, CONJUGATIVE PLASMID, PROVIDES EVIDENCE
journal title
GENETICS
Genetics
volume
178
issue
4
pages
2179 - 2190
Web of Science type
Article
Web of Science id
000255239600028
JCR category
GENETICS & HEREDITY
JCR impact factor
4.002 (2008)
JCR rank
34/138 (2008)
JCR quartile
1 (2008)
ISSN
0016-6731
DOI
10.1534/genetics.107.084475
language
English
UGent publication?
no
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
765524
handle
http://hdl.handle.net/1854/LU-765524
date created
2009-10-19 16:47:43
date last changed
2016-12-19 15:41:04
@article{765524,
  abstract     = {Little is known about the range of hosts in which broad-host-range (BHR) plasmids can persist in the absence of selection for plasmid-encoded traits, and whether this {\textacutedbl}long-term host range{\textacutedbl} can evolve over time. Previously, the BHR multidrug resistance plasmid pB10 was shown to be highly unstable in Stenotrophomonas maltophilia P21 and Pseudomonas putida H2. To investigate whether this plasmid can adapt to such unfavorable hosts, we performed evolution experiments wherein pB10 was maintained in strain P21, strain H2, and alternatingly in P21 and H2. Plasmids that evolved in P21 and in both hosts showed increased stability and decreased cost in ancestral host P21. However, the latter group showed higher variability in stability patterns, suggesting that regular switching between distinct hosts hampered adaptive plasmid evolution. The plasmids evolved in P21 were also equally or more stable in other hosts compared to pB10, which suggested true host-range expansion. The complete genome sequences of four evolved plasmids with improved stability showed only one or two genetic changes. The stability of plasmids evolved in H2 improved only in their coevolved hosts, not in the ancestral host. Thus a BHR plasmid can adapt to an unfavorable host and thereby expand its long-term host range.},
  author       = {De Gelder, Leen and Williams, Julia J and Ponciano, Jos{\'e} M and Sota, Masahiro and Top, Eva M},
  issn         = {0016-6731},
  journal      = {GENETICS},
  keyword      = {PB10,SELECTION,POPULATION,HORIZONTAL GENE-TRANSFER,GRAM-NEGATIVE BACTERIA,RESISTANCE PLASMIDS,ACTIVATED-SLUDGE,BENEFICIAL MUTATIONS,CONJUGATIVE PLASMID,PROVIDES EVIDENCE},
  language     = {eng},
  number       = {4},
  pages        = {2179--2190},
  title        = {Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid},
  url          = {http://dx.doi.org/10.1534/genetics.107.084475},
  volume       = {178},
  year         = {2008},
}

Chicago
De Gelder, Leen, Julia J Williams, José M Ponciano, Masahiro Sota, and Eva M Top. 2008. “Adaptive Plasmid Evolution Results in Host-range Expansion of a Broad-host-range Plasmid.” Genetics 178 (4): 2179–2190.
APA
De Gelder, L., Williams, J. J., Ponciano, J. M., Sota, M., & Top, E. M. (2008). Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid. GENETICS, 178(4), 2179–2190.
Vancouver
1.
De Gelder L, Williams JJ, Ponciano JM, Sota M, Top EM. Adaptive plasmid evolution results in host-range expansion of a broad-host-range plasmid. GENETICS. 2008;178(4):2179–90.
MLA
De Gelder, Leen, Julia J Williams, José M Ponciano, et al. “Adaptive Plasmid Evolution Results in Host-range Expansion of a Broad-host-range Plasmid.” GENETICS 178.4 (2008): 2179–2190. Print.