Impact of conjugal transfer on the stability of IncP-1 plasmid pKJK5 in bacterial populations

Bahl, Martin Iain; Hansen, Lars Hestbjerg; Sørensen, Søren J.

doi:10.1111/j.1574-6968.2006.00536.x

Cited by 52 publications

(35 citation statements)

References 18 publications

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“…Our data show community-wide access to beneficial accessory genes resulting from processes occurring in one species in that community, specifically the persistence of a conjugative plasmid by infection. This extends previous evidence demonstrating the invasion and survival of plasmids as infectious parasitic elements, especially in spatially structured populations (11,26,37).…”

Section: Discussionsupporting

confidence: 89%

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Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

Hall

Wood

Harrison

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

164

230

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Horizontal gene transfer is a fundamental process in bacterial evolution that can accelerate adaptation via the sharing of genes between lineages. Conjugative plasmids are the principal genetic elements mediating the horizontal transfer of genes, both within and between bacterial species. In some species, plasmids are unstable and likely to be lost through purifying selection, but when alternative hosts are available, interspecific plasmid transfer could counteract this and maintain access to plasmid-borne genes. To investigate the evolutionary importance of alternative hosts to plasmid population dynamics in an ecologically relevant environment, we established simple soil microcosm communities comprising two species of common soil bacteria, Pseudomonas fluorescens and Pseudomonas putida, and a mercury resistance (Hg R ) plasmid, pQBR57, both with and without positive selection [i.e., addition of Hg(II)]. In single-species populations, plasmid stability varied between species: although pQBR57 survived both with and without positive selection in P. fluorescens, it was lost or replaced by nontransferable Hg R captured to the chromosome in P. putida. A simple mathematical model suggests these differences were likely due to pQBR57's lower intraspecific conjugation rate in P. putida. By contrast, in two-species communities, both models and experiments show that interspecific conjugation from P. fluorescens allowed pQBR57 to persist in P. putida via source-sink transfer dynamics. Moreover, the replacement of pQBR57 by nontransferable chromosomal Hg R in P. putida was slowed in coculture. Interspecific transfer allows plasmid survival in host species unable to sustain the plasmid in monoculture, promoting community-wide access to the plasmid-borne accessory gene pool and thus potentiating future evolvability.horizontal gene transfer | plasmids | mobile genetic elements | microbial ecology

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Section: Discussionsupporting

confidence: 89%

“…Plasmids can also be maintained within a host species as infectious elements, provided conjugation rates are high (e.g., ref. 11). …”

mentioning

confidence: 99%

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

Hall

Wood

Harrison

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

164

230

View full text Add to dashboard Cite

show abstract

“…However, these simulations represent only one of a variety of possible plasmid-host-environment combinations. The success of actual plasmid invasions is mainly determined by plasmid cost, host density and conjugation rates (Levin et al, 1979;Lundquist and Levin, 1986;Turner, 2004;Bahl et al, 2007). We therefore wished to determine and compare the effects of bacterial density and plasmid cost on invasion by P fin þ and P finÀ , which represent plasmids with differing conjugation rates.…”

Section: Resultsmentioning

confidence: 99%

“…Bacteria and their conjugative plasmids can also provide a tractable model of a host-parasite system. These genetic elements can persist in suitable hosts for many generations without conferring a selective advantage (Turner et al, 2002;Dahlberg and Chao, 2003;De Gelder et al, 2004;Bahl et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Competition favours reduced cost of plasmids to host bacteria

2009

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Conjugative plasmids of Gram-negative bacteria have both vertical and horizontal modes of transmission: they are segregated to daughter cells during division, and transferred between hosts by plasmid-encoded conjugative machinery. Despite maintaining horizontal mobility, many plasmids carry fertility inhibition (fin) systems that repress their own conjugative transfer. To assess the ecological basis of self-transfer repression, we compared the invasion of bacterial populations by fin þ and fin À variants of the plasmid R1 using a computational model and co-culture competitions. We observed that the fin þ variant had a modest cost to the host (measured by reduction in growth rate), while the fin À variant incurred a larger cost. In simulations and empirical competitions the fin À plasmid invaded cultures quickly, but was subsequently displaced by the fin þ plasmid. This indicated a competitive advantage to reducing horizontal transmission and allowing increased host replication. Computational simulations predicted that the advantage associated with reduced cost to the host would be maintained over a wide range of environmental conditions and plasmid costs. We infer that vertical transmission in concert with competitive exclusion favour decreased horizontal mobility of plasmids. Similar dynamics may exert evolutionary pressure on parasites, such as temperate bacteriophages and vertically transmitted animal viruses, to limit their rates of horizontal transfer.

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“…Furthermore, the studies of Bergstrom et al (2000) are based on transfer rates in liquid culture and do not take into account that natural bacterial communities commonly exist as biofilms, where cell densities and hence rates of infectious transfer are expected to be much higher (Sorensen et al 2005). There is some recent strong evidence in support of transfer rates being sufficient to support plasmid populations on bacterial mats (Bahl et al 2007) and on rat endothelial cells (Bahl et al 2006). Indeed the ability to form biofilm may be conferred by the plasmid itself, thus providing a means by which the plasmid may be maintained though high rates of transfer in addition to allowing the bacteria to survive harsh environments (Imran et al 2005).…”

mentioning

confidence: 99%

The Persistence of Parasitic Plasmids

Lili¹,

Britton²,

Feil

2007

Genetics

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The conditions under which plasmids are predicted to persist remain controversial. Here, we reevaluate the ordinary differential equations used previously to model plasmid persistence and conclude that the parameter space required for maintenance is far less stringent than has been supposed. Strikingly, our model demonstrates that purely parasitic plasmids may persist, even in the absence of heterogeneity in the host population, and that this persistence is expressed by oscillations or damped oscillations between the plasmid-bearing and the plasmid-free class.

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Impact of conjugal transfer on the stability of IncP-1 plasmid pKJK5 in bacterial populations

Cited by 52 publications

References 18 publications

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities

Competition favours reduced cost of plasmids to host bacteria

The Persistence of Parasitic Plasmids

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