The Evolution and Regulation of Morphological Complexity in the Vibrios

Abstract

Like all life forms, bacteria come in many shapes and sizes that evolved in response to their evolutionary niches. Bacterial morphology is defined by a peptidoglycan (PG) cell wall and the cytoskeleton-guided PG synthesis machinery that builds rod shape cells is well-studied. In contrast, we lack an understanding of how more complex bacterial morphologies are built, how complex shape determinants may interact with the rod-determining machinery, and how complex morphologies can arise de novo. Here, we study the curved pandemic pathogen Vibrio cholerae as a model for cell shape complexity. We demonstrate that two proteins, CrvA and CrvB, are the only Vibrio-specific factors required for cell curvature by using them to artificially induce cell curvature in Escherichia coli, Pseudomonas aeruginosa, Caulobacter crescentus, and Agrobacterium tumefaciens. Characterization of CrvA/B in V. cholerae, E. coli¸ and in vitro revealed that CrvA/B act as a modular unit that acts autonomously of the cytoskeleton-guided PG synthesis machinery by assembling periplasmic filaments that can bind directly to the cell wall to locally limit cell wall growth. Furthermore, we investigated the unique contributions of CrvA and CrvB to filament formation and curvature. This uncovered a potential evolutionary trajectory for the crv genes wherein crvA and crvB arose through partial duplication of an ancestral hybrid gene followed by specialization that promotes rapid changes in cell curvature. The modular, cytoskeleton-autonomous nature of CrvA/B demonstrates that bacterial morphology is more plastic than previously appreciated and suggests that cell shape complexity can arise without the coevolution of integral cell biological components.