Multi-host environments select for host-generalist conjugative plasmids

Kottara, Anastasia; Hall, James P. J.; Harrison, Ellie; Brockhurst, Michael A.

doi:10.1186/s12862-016-0642-z

Cited by 19 publications

(16 citation statements)

References 27 publications

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“…Interspecific conjugation also provides opportunity for plasmid recombination with resident genetic elements, enhancing genomic diversification (2). Furthermore, prolonged source-sink transfer dynamics could promote plasmid host range expansion (30), as also shown for bacteriophage (31). Previously, Dionisio et al (32) noted how multispecies communities might accelerate plasmid spread when a highly conjugative intermediate species enhances plasmid transfer between two poorly conjugative species.…”

Section: Discussionmentioning

confidence: 93%

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.

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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: Discussionmentioning

confidence: 93%

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.

Self Cite

169

230

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“…When selecting for delayed transmission times, extracellular survival improved, but viral fecundity decreased (393), while adaptation to a high multiplicity of infection resulted in lower success at a low multiplicity of infection (394). Adaptation of plasmids highly resembles the evolution of viruses, with trade-offs toward hosts that were not encountered during adaptive evolution (395,396). The LTEE displayed an extreme example of specific trade-off by specialism.…”

Section: Pervasive Trade-offs and Specialists In Experimental Evolutionmentioning

confidence: 99%

Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution

Bergh

Swings

Fauvart

et al. 2018

Microbiol Mol Biol Rev

163

164

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In experimental evolution, laboratory-controlled conditions select for the adaptation of species, which can be monitored in real time. Despite the current popularity of such experiments, nature's most pervasive biological force was long believed to be observable only on time scales that transcend a researcher's life-span, and studying evolution by natural selection was therefore carried out solely by comparative means. Eventually, microorganisms' propensity for fast evolutionary changes proved us wrong, displaying strong evolutionary adaptations over a limited time, nowadays massively exploited in laboratory evolution experiments. Here, we formulate a guide to experimental evolution with microorganisms, explaining experimental design and discussing evolutionary dynamics and outcomes and how it is used to assess ecoevolutionary theories, improve industrially important traits, and untangle complex phenotypes. Specifically, we give a comprehensive overview of the setups used in experimental evolution. Additionally, we address population dynamics and genetic or phenotypic diversity during evolution experiments and expand upon contributing factors, such as epistasis and the consequences of (a)sexual reproduction. Dynamics and outcomes of evolution are most profoundly affected by the spatiotemporal nature of the selective environment, where changing environments might lead to generalists and structured environments could foster diversity, aided by, for example, clonal interference and negative frequency-dependent selection. We conclude with future perspectives, with an emphasis on possibilities offered by fast-paced technological progress. This work is meant to serve as an introduction to those new to the field of experimental evolution, as a guide to the budding experimentalist, and as a reference work to the seasoned expert.

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“…Given that positive selection cannot explain the long-term stability of costly plasmids ( Hall et al, 2017 ), the explanation for such long-term stability remains a most challenging task, since segregational loss and the cost of plasmid carriage should drive the loss of plasmids through purifying selection ( Hall et al, 2017 ). In this respect, two evolutionary routes to plasmid stability appear possible ( Hall et al, 2017 ): (i) the evolution of high conjugation rates would allow plasmids to survive as infectious agents through horizontal transmission ( Hall et al, 2016 ; Kottara et al, 2016 ); and (ii) compensatory evolution to ameliorate the cost of plasmid carriage can weaken purifying selection against the plasmid backbone ( Harrison et al, 2015 ; Porse et al, 2016 ).…”

Section: Effect Of Plasmid Acquisition On Host Fitnessmentioning

confidence: 99%

Plasmid-Mediated Bioaugmentation for the Bioremediation of Contaminated Soils

et al. 2017

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Bioaugmentation, or the inoculation of microorganisms (e.g., bacteria harboring the required catabolic genes) into soil to enhance the rate of contaminant degradation, has great potential for the bioremediation of soils contaminated with organic compounds. Regrettably, cell bioaugmentation frequently turns into an unsuccessful initiative, owing to the rapid decrease of bacterial viability and abundance after inoculation, as well as the limited dispersal of the inoculated bacteria in the soil matrix. Genes that encode the degradation of organic compounds are often located on plasmids and, consequently, they can be spread by horizontal gene transfer into well-established, ecologically competitive, indigenous bacterial populations. Plasmid-mediated bioaugmentation aims to stimulate the spread of contaminant degradation genes among indigenous soil bacteria by the introduction of plasmids, located in donor cells, harboring such genes. But the acquisition of plasmids by recipient cells can affect the host’s fitness, a crucial aspect for the success of plasmid-mediated bioaugmentation. Besides, environmental factors (e.g., soil moisture, temperature, organic matter content) can play important roles for the transfer efficiency of catabolic plasmids, the expression of horizontally acquired genes and, finally, the contaminant degradation activity. For plasmid-mediated bioaugmentation to be reproducible, much more research is needed for a better selection of donor bacterial strains and accompanying plasmids, together with an in-depth understanding of indigenous soil bacterial populations and the environmental conditions that affect plasmid acquisition and the expression and functioning of the catabolic genes of interest.

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Multi-host environments select for host-generalist conjugative plasmids

Cited by 19 publications

References 27 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

Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution

Plasmid-Mediated Bioaugmentation for the Bioremediation of Contaminated Soils

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