Streptomyces venezuelae exploration: redefining growth in polar-growing bacteria

Abstract

Streptomyces venezuelae employs two modes of development, classical growth and exploration. The newly described ‘exploratory’ growth occurs in response to glucose depletion and can occur in response to amino acid abundance. It begins with spore germination and vegetative outgrowth, but instead of then raising aerial hyphae and sporulating, S. venezuelae initiates rapid colony expansion that is driven by vegetative-like exploring hyphae. In classical development, vegetative hyphae grow by tip extension, which is mediated by the essential protein DivIVA. DivIVA localizes to the hyphal tips and recruits the cell wall biosynthetic machinery to drive growth at the cell poles. Our data indicate that while exploring hyphae are still polar-growing, DivIVA is subject to a novel proteolytic event during exploration. Furthermore, our investigations into the nature of the cell wall peptidoglycan of exploring cells have identified key changes to both its composition and structure. Specifically, the peptidoglycan isolated from explorers has a unique crosslinking pattern. Exploring cell walls further displayed remarkable structural plasticity; early-stage exploring cells have unusually thin hyphal walls that increase in thickness as exploration proceeds. Intriguingly, this cell wall thickening depends on MreB, a key shape-determining factor in many rod-shaped bacteria. mreB mutants exhibit defects in exploratory growth and increased cell lysis. In addition to having thinner cell walls, mreB mutants also have an altered peptidoglycan profile that suggests a disordered synthesis program and employ an unusual pattern of cell wall synthesis based on fluorescent D-amino acid incorporation. Our work is showing that S. venezuelae can radically reconfigure their cell wall construction from purely polar growth to a combination of polar growth and MreB-guided lateral wall insertion. This work reveals unprecedented flexibility in bacterial cell wall biosynthetic capabilities.