Community-wide plasmid gene mobilization and selection

Sentchilo, Vladimir; Mayer, Antonia P.; Guy, Lionel; Miyazaki, Ryo; Tringe, Susannah G.; Barry, Kerrie; Malfatti, Stephanie; Goessmann, Alexander; Robinson‐Rechavi, Marc; Meer, Jan Roelof van der

doi:10.1038/ismej.2013.13

Cited by 117 publications

(118 citation statements)

References 52 publications

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“…However, these studies have primarily been conducted in one-plasmid/one-host systems, which are not reflective of natural microbial populations containing many different bacterial species (40) and mobile genetic elements (21,41). We have shown that even simple two-species microbial communities offer evolutionary opportunities unavailable in a single-species population.…”

Section: Discussionmentioning

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.

158

225

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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: 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.

158

225

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“…However, from the multitude of ARGs found in wastewater treatment plants (Sentchilo et al . ), only few persist in the natural environment (Auerbach et al . ).…”

Section: Discussionmentioning

confidence: 99%

Constitutive presence of antibiotic resistance genes within the bacterial community of a large subalpine lake

et al. 2015

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The fate of antibiotic resistance genes (ARGs) in environmental microbial communities is of primary concern as prodromal of a potential transfer to pathogenic bacteria. Although of diverse origin, the persistence of ARGs in aquatic environments is highly influenced by anthropic activities, allowing potential control actions in well-studied environments. However, knowledge of abundance and space-time distribution of ARGs in ecosystems is still scarce. Using quantitative real-time PCR, we investigated the presence and the abundance of twelve ARGs (against tetracyclines, β-lactams, aminoglycosides, quinolones and sulphonamides) at different sampling sites, depths and seasons, in Lake Maggiore, a large subalpine lake, and in the area of its watershed. We then evaluated the correlation between each ARG and a number of ecological parameters in the water column in the deepest part of the lake. Our results suggest the constitutive presence of at least four ARGs within the bacterial community with a high proportion of bacteria potentially resistant to tetracyclines and sulphonamides. The presence of these ARGs was independent of the total bacterial density and temperature. The dynamics of tet(A) and sulII genes were, however, positively correlated with dissolved oxygen and negatively to chlorophyll a, suggesting that the resistant microbes inhabit specific niches. These observations indicate that the lake is a reservoir of antibiotic resistances, highlighting the need of a deeper understanding of the sources of ARGs and the factors allowing their persistence in waters.

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“…Plasmids are hugely diverse in terms of their size (Smillie et al ., ) and the genes that they contain; a large number of sequenced plasmid genes have no similarity to previously sequenced genes and a high proportion are of unknown function (e.g. Tett et al ., ; Sentchilo et al ., ; Xiong et al ., ). Plasmids represent a vast pool of genetic diversity on which bacterial communities can draw, and understanding plasmid biology is central to understanding microbial evolution and ecology.…”

Section: Introductionmentioning

confidence: 99%

Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects

Hall

Harrison

Lilley

et al. 2015

Environmental Microbiology

111

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SummaryPlasmids are important mobile elements that can facilitate genetic exchange and local adaptation within microbial communities. We compared the sequences of four co‐occurring pQBR family environmental mercury resistance plasmids and measured their effects on competitive fitness of a P seudomonas fluorescens SBW25 host, which was isolated at the same field site. Fitness effects of carriage differed between plasmids and were strongly context dependent, varying with medium, plasmid status of competitor and levels of environmental mercury. The plasmids also varied widely in their rates of conjugation and segregational loss. We found that few of the plasmid‐borne accessory genes could be ascribed functions, although we identified a putative chemotaxis operon, a type IV pilus‐encoding cluster and a region encoding putative arylsulfatase enzymes, which were conserved across geographically distant isolates. One plasmid, pQBR55, conferred the ability to catabolize sucrose. Transposons, including the mercury resistance Tn5042, appeared to have been acquired by different pQBR plasmids by recombination, indicating an important role for horizontal gene transfer in the recent evolution of pQBR plasmids. Our findings demonstrate extensive genetic and phenotypic diversity among co‐occurring members of a plasmid community and suggest a role for environmental heterogeneity in the maintenance of plasmid diversity.

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Community-wide plasmid gene mobilization and selection

Cited by 117 publications

References 52 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

Constitutive presence of antibiotic resistance genes within the bacterial community of a large subalpine lake

Environmentally co‐occurring mercury resistance plasmids are genetically and phenotypically diverse and confer variable context‐dependent fitness effects

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