Characterization of pNI10 plasmid in Pseudomonas, and the construction of an improved Escherichia and Pseudomonas shuttle vector, pNUK73

Kawanami, Takafumi; Nitta, C.; Iwata, N.; Usami, Shoji; Abe, Yoshinobu; Koide, Yoshinobu

doi:10.1007/s00253-002-1195-1

Cited by 9 publications

(7 citation statements)

References 22 publications

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“…We developed an experimental model system using P. aeruginosa strain PAO1 transformed with pNUK73, which is a small, multi-copy, non-transmissible plasmid carrying an aminoglycoside 3′-phosphotransferase, which confers resistance to kanamycin and neomycin 28 . The stability of non-transmissible plasmids in a bacterial population, in the absence of positive selection, depends on two factors: (i) the rate of segregational loss and (ii) the cost of plasmid carriage 29 .…”

Section: Resultsmentioning

confidence: 99%

“…In this paper we investigate how compensatory adaptation and rare episodes of positive selection for plasmid-encoded genes influence the persistence of non-transmissible plasmids at the population level. To address this problem, we combine an experimental model using the opportunistic pathogen Pseudomonas aeruginosa and the small non-transmissible plasmid pNUK73 28 with mathematical modelling and whole genome sequencing. We show that rare events of selection for plasmid-encoded traits interact with a rapid compensatory adaptation and are sufficient to maintain the plasmid in the population for hundreds of generations.…”

Section: Introductionmentioning

confidence: 99%

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Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids

et al. 2014

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Plasmids are important drivers of bacterial evolution, but it is challenging to understand how plasmids persist over the long term because plasmid carriage is costly. Classical models predict that horizontal transfer is necessary for plasmid persistence, but recent work shows that almost half of plasmids are non-transmissible. Here we use a combination of mathematical modelling and experimental evolution to investigate how a costly, nontransmissible plasmid, pNUK73, can be maintained in populations of Pseudomonas aeruginosa. Compensatory adaptation increases plasmid stability by eliminating the cost of plasmid carriage. However, positive selection for plasmid-encoded antibiotic resistance is required to maintain the plasmid by offsetting reductions in plasmid frequency due to segregational loss. Crucially, we show that compensatory adaptation and positive selection reinforce each other's effects. Our study provides a new understanding of how plasmids persist in bacterial populations, and it helps to explain why resistance can be maintained after antibiotic use is stopped.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids

et al. 2014

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“…PA4673.15 itself was also underexpressed, albeit non-significantly, suggesting that PA4673.15 regulates the expression of both kinases. The pNUK73 small plasmid carries the backbone of the natural cryptic plasmid pNI10 isolated from Pseudomonas fulva 21 and codes for three genes, namely the Rep plasmid replication protein gene from pNI10 ( rep ), an aminoglycoside 3′-phosphotransferase gene ( aphA1 , which confers resistance to kanamycin and neomycin) and a lacZ reporter gene (Fig. 2B).…”

Section: Resultsmentioning

confidence: 99%

Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa

et al. 2015

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Horizontal gene transfer (HGT) plays a key role in bacterial evolution, especially with respect to antibiotic resistance. Fitness costs associated with mobile genetic elements (MGEs) are thought to constrain HGT, but our understanding of these costs remains fragmentary, making it difficult to predict the success of HGT events. Here we use the interaction between P. aeruginosa and a costly plasmid (pNUK73) to investigate the molecular basis of the cost of HGT. Using RNA-Seq, we show that the acquisition of pNUK73 results in a profound alteration of the transcriptional profile of chromosomal genes. Mutations that inactivate two genes encoded on chromosomally integrated MGEs recover these fitness costs and transcriptional changes by decreasing the expression of the pNUK73 replication gene. Our study demonstrates that interactions between MGEs can compromise bacterial fitness via altered gene expression, and we argue that conflicts between mobile elements impose a general constraint on evolution by HGT.

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“…To investigate interactions between plasmids, we used six plasmids that are able to replicate in Pseudomonas and were recovered from different sources, including five large plasmids from a diverse range of incompatibility groups: pBS228, Rms149, pAKD1, PAMBL-1 and PAMBL-2, and a single small plasmid pNI105 (Itoh et al , 1991, 2003; Haines et al , 2005, 2007; Tato et al , 2010; Sen et al , 2011) (Table 1). The five large plasmids range in size from 30 to 90 kb and confer resistance to a wide variety of antibiotics and the heavy metal mercury (Table 1).…”

Section: Resultsmentioning

confidence: 99%

Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations

2013

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Plasmids have a key role in the horizontal transfer of genes among bacteria. Although plasmids are catalysts for bacterial evolution, it is challenging to understand how they can persist in bacterial populations over the long term because of the burden they impose on their hosts (the ‘plasmid paradox'). This paradox is especially perplexing in the case of ‘small' plasmids, which are unable to self-transfer by conjugation. Here, for the first time, we investigate how interactions between co-infecting plasmids influence plasmid persistence. Using an experimental model system based on interactions between a diverse assemblage of ‘large' plasmids and a single small plasmid, pNI105, in the pathogenic bacterium Pseudomonas aeruginosa, we demonstrate that positive epistasis minimizes the cost associated with carrying multiple plasmids over the short term and increases the stability of the small plasmid over a longer time scale. In support of these experimental data, bioinformatic analysis showed that associations between small and large plasmids are more common than would be expected owing to chance alone across a range of families of bacteria; more generally, we find that co-infection with multiple plasmids is more common than would be expected owing to chance across a wide range of bacterial phyla. Collectively, these results suggest that positive epistasis promotes plasmid stability in bacterial populations. These findings pave the way for future mechanistic studies aimed at elucidating the molecular mechanisms of plasmid–plasmid interaction, and evolutionary studies aimed at understanding how the coevolution of plasmids drives the spread of plasmid-encoded traits.

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Characterization of pNI10 plasmid in Pseudomonas, and the construction of an improved Escherichia and Pseudomonas shuttle vector, pNUK73

Cited by 9 publications

References 22 publications

Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids

Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids

Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa

Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations

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