Positive selection inhibits gene mobilization and transfer in soil bacterial communities

Abstract

Horizontal gene transfer (HGT) between bacterial lineages is a fundamental evolutionary process that accelerates adaptation. Sequence analyses show that conjugative plasmids are principal agents of HGT in natural communities. However, we lack understanding of how the ecology of bacterial communities and their environments affect the dynamics of plasmid-mediated gene mobilization and transfer. Here we show, in simple experimental soil bacterial communities containing a conjugative mercury resistance plasmid, the repeated, independent mobilization of transposon-borne genes from chromosome to plasmid, plasmid to chromosome and, in the absence of mercury selection, interspecific gene transfers from the chromosome of one species to the other via the plasmid. By reducing conjugation, positive selection for plasmid-encoded traits, like mercury resistance, can consequently inhibit HGT. Our results suggest that interspecific plasmid-mediated gene mobilization is most likely to occur in environments where plasmids are infectious, parasitic elements rather than those where plasmids are positively selected, beneficial elements.

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Fig. 1: Evolved clones show extensive within- and between-species gene mobilization.
Fig. 2: Plasmid dynamics are altered under positive selection.
Fig. 3: Spread of chromosomally acquired mercury resistance.

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Acknowledgements

We thank P. Koldkjaer and others at the Liverpool Centre for Genomic Research for assistance with sample preparation and sequencing. This work was supported by ERC Grant Agreement no. 311490-COEVOCON to M.A.B. and a Philip Leverhulme Prize from Leverhulme Trust to M.A.B.

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J.P.J.H., E.H. and M.A.B. designed the study; J.P.J.H. collected data; J.P.J.H., D.W. and S.P. analysed the data. J.P.J.H. and M.A.B. drafted the manuscript. All authors discussed results and commented on the manuscript.

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Correspondence to James P. J. Hall or Michael A. Brockhurst.

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Hall, J.P.J., Williams, D., Paterson, S. et al. Positive selection inhibits gene mobilization and transfer in soil bacterial communities. Nat Ecol Evol 1, 1348–1353 (2017). https://doi.org/10.1038/s41559-017-0250-3

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