A mechanism for FtsZ-independent proliferation in Streptomyces

Fernando Santos-Beneit,David M Roberts,Stuart Cantlay,Joseph R Mccormick,Jeff Errington

doi:10.1038/s41467-017-01596-z

Fernando Santos-Beneit, David M Roberts + Show 3 more

Open Access

https://doi.org/10.1038/s41467-017-01596-z

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Journal: Nature Communications	Publication Date: Nov 9, 2017
Citations: 29	License type: open-access

Affiliation: Newcastle University, Duquesne University

Abstract

The central player in bacterial cell division, FtsZ, is essential in almost all organisms in which it has been tested, with the most notable exception being Streptomyces. Streptomycetes differ from many bacteria in growing from the cell tip and undergoing branching, similar to filamentous fungi. Here we show that limited cell damage, either mechanical or enzymatic, leads to near complete destruction of mycelial microcolonies of a Streptomyces venezuelae ftsZ mutant. This result is consistent with a lack of ftsZ-dependent cross-walls and may be inconsistent with a recently proposed role for membrane structures in the proliferation of ftsZ mutants in other Streptomyces species. Rare surviving fragments of mycelium, usually around branches, appear to be the preferred sites of resealing. Restoration of growth in hyphal fragments of both wild-type and ftsZ mutant hyphae can occur at multiple sites, via branch-like outgrowths containing DivIVA protein at their tips. Thus, our results highlight branching as a means of FtsZ-independent cell proliferation.

Highlights

The central player in bacterial cell division, FtsZ, is essential in almost all organisms in which it has been tested, with the most notable exception being Streptomyces
The membrane follows the shape of the cell, which is in turn determined by the peptidoglycan cell wall
The ftsZ genes of both S. venezuelae (SVEN_1737) and S. coelicolor (SCO2082) are located in highly conserved gene clusters (SVEN_1732-47 and SCO2077-92, respectively) coding for proteins required for efficient growth and branching, sporulation and cell-wall precursor synthesis

Summary

Introduction

The central player in bacterial cell division, FtsZ, is essential in almost all organisms in which it has been tested, with the most notable exception being Streptomyces. We show that limited cell damage, either mechanical or enzymatic, leads to near complete destruction of mycelial microcolonies of a Streptomyces venezuelae ftsZ mutant This result is consistent with a lack of ftsZ-dependent cross-walls and may be inconsistent with a recently proposed role for membrane structures in the proliferation of ftsZ mutants in other Streptomyces species. We recently showed that ftsZ can be deleted in Escherichia coli, but only after introduction of one or more compensating mutations that enable the switch to a very bizarre ‘coliflower’ morphology[6] Actinomycetes such as Streptomyces form an unusual branching mycelium in which cross-walls (dependent on FtsZ) form relatively infrequently[7]. A novel form of cytoplasmic compartmentalisation based on complex membrane invaginations or cross-membranes has been described in Streptomyces, and reported to contribute to the proliferation of ftsZ mutants[9,10]. Our results suggest that the habit of streptomycetes to form hyphae that grow from the cell tip, together with their ability to form branched structures by generating new tips, contribute to their ability to survive fragmentation and for the fragments to resume growth

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