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Adaptive evolution by spontaneous domain fusion and protein relocalization

Abstract

Knowledge of adaptive processes encompasses understanding the emergence of new genes. Computational analyses of genomes suggest that new genes can arise by domain swapping; however, empirical evidence has been lacking. Here we describe a set of nine independent deletion mutations that arose during selection experiments with the bacterium Pseudomonas fluorescens in which the membrane-spanning domain of a fatty acid desaturase became translationally fused to a cytosolic di-guanylate cyclase, generating an adaptive ‘wrinkly spreader’ phenotype. Detailed genetic analysis of one gene fusion shows that the mutant phenotype is caused by relocalization of the di-guanylate cyclase domain to the cell membrane. The relative ease by which this new gene arose, along with its functional and regulatory effects, provides a glimpse of mutational events and their consequences that are likely to have a role in the evolution of new genes.

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Fig. 1: Numerous mutational routes activating cellulose over-production underpin the WS phenotype.
Fig. 2: Arrangement of pflu0184 and pflu0183 in the ancestral smooth genotype and following gene fusion.
Fig. 3: Transcription of fwsR from the fadA promoter is insufficient to cause FWS.
Fig. 4: The FWS phenotype requires translational fusion of the fadA and fwsR genes.
Fig. 5: Fluorescence microscopy depicting the distribution of GFP-tagged proteins encoded from the fwsR locus.
Fig. 6: Translational fusion of the transmembrane regions of mwsR to fwsR causes the FWS phenotype.

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Acknowledgements

This work was supported in part by Marsden Fund Council from New Zealand Government funding (administered by the Royal Society of New Zealand) and the New Zealand Institute for Advanced Study. We thank J. Gallie and P. Lind for discussion and comments on the manuscript and H. Hendrickson for assistance with microscopy.

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A.D.F. and P.B.R. conceived and designed the study. A.D.F. and P.R. acquired the data. All authors analysed and interpreted the data. A.D.F. and P.B.R. drafted and revised the paper.

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Correspondence to Paul B. Rainey.

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Farr, A.D., Remigi, P. & Rainey, P.B. Adaptive evolution by spontaneous domain fusion and protein relocalization. Nat Ecol Evol 1, 1562–1568 (2017). https://doi.org/10.1038/s41559-017-0283-7

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