Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations

Fox, Randal; Zhang, Xue; Krone, Stephen M.; Top, Eva M.

doi:10.1038/ismej.2008.53

Cited by 99 publications

(137 citation statements)

References 50 publications

(43 reference statements)

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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: 75%

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: 75%

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

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“…Also, structured environments allowing the development of aggregates or biofilms can increase the spread of wild-type conjugative plasmids in bacterial populations (Molin and Tolker-Nielsen, 2003). Our model assumes mass-action kinetics associated with well-mixed populations; the kinetics of plasmid spread can be quite different on surfaces (Simonsen, 1990;Krone et al, 2007;Fox et al, 2008).…”

Section: Discussionmentioning

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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“…However, many mobile elements do exert costs on their hosts (Diaz Ricci and Hernandez, 2000;Fox et al, 2008), raising the question as to how costly and poorly transmissible MGEs can persist within a genome Stewart and Levin, 1977;Bergstrom et al, 2000;Lili et al, 2007). Stewart and Levin (1977) built one of the first models to analyse plasmid persistence, and argued that plasmids could not persist under low rates of HGT.…”

Section: Introductionmentioning

confidence: 99%