What mechanisms underlie the transitions responsible for the diverse shapes observed in the living world? Although bacteria exhibit a myriad of morphologies1, the mechanisms responsible for the evolution of bacterial cell shape are not understood. We investigated morphological diversity in a group of bacteria that synthesize an appendage-like extension of the cell envelope called the stalk2,3. The location and number of stalks varies among species, as exemplified by three distinct subcellular positions of stalks within a rod-shaped cell body: polar in the genus Caulobacter and subpolar or bilateral in the genus Asticcacaulis4. Here we show that a developmental regulator of Caulobacter crescentus, SpmX5, is co-opted in the genus Asticcacaulis to specify stalk synthesis either at the subpolar or bilateral positions. We also show that stepwise evolution of a specific region of SpmX led to the gain of a new function and localization of this protein, which drove the sequential transition in stalk positioning. Our results indicate that changes in protein function, co-option and modularity are key elements in the evolution of bacterial morphology. Therefore, similar evolutionary principles of morphological transitions apply to both single-celled prokaryotes and multicellular eukaryotes.
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Genomic data of strains sequenced in this study are deposited in GenBank/EMBL/DDBJ under accession numbers AWGD00000000 (Asticcacaulis sp. AC460), AWGE00000000 (Asticcacaulis sp. AC466), AWGC00000000 (Asticcacaulis sp. AC402), AWGF00000000 (Asticcacaulis sp. YBE204) and AWGB00000000 (Asticcacaulis benevestitus DSM16100).
We thank members of the Brun laboratory and C. Fuqua for comments on the manuscript. We thank D. Kysela, V. Hughes and V. Silvanose for help in environmental sampling and phylogenetic analysis, L. Zhuo and C. Huang for help in statistical analysis, S. Shaw for advice on quantitative image analysis, M. Hahn, M. Lynch and R. Raff for discussions on evolution, and the Center for Genomics and Bioinformatics at Indiana University for help in sequencing. We thank the Indiana University Light Microscopy Imaging Center for their help with OMX super-resolution microscopy, supported by National Institutes of Health grant S10RR028697-01, and the Indiana Molecular biology Institute electron microscopy facility at Indiana University for their help with electron microscopy. We thank M. Thanbichler, J. Poindexter, P. Caccamo and P. Viollier for providing us with Caulobacter strain and plasmids, J. Poindexter, J. Peterson, J. Lindquist and A. Quinones for help in locating the strain collection of the late Jack Pate from which we obtained some of the A. excentricus and A. biprosthecum strains used in this study, and M. Wortinger, S. Green, E. Quardokus and J. (Wagner) Herman for early work with Asticcacaulis that helped set the stage for this study. This work was supported by National Institutes of Health grant GM051986, National Science Foundation grant MCB0731950 and by a grant from the Indiana University Metabolomics and Cytomics Initiative (METACyt) program, which was financed, in part, by a major endowment from the Lilly Foundation. P.J.B.B. was supported by National Institutes of Health National Research Service Award AI072992.
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A PopZ‐linked apical recruitment assay for studying protein–protein interactions in the bacterial cell envelope
Molecular Microbiology (2019)