FtsZ of Filamentous, Heterocyst-Forming Cyanobacteria Has a Conserved N-Terminal Peptide Required for Normal FtsZ Polymerization and Cell Division

Laura Corrales-Guerrero,Sergio Camargo,Jesús A G Ochoa De Alda,Ana Valladares,Antonia Herrero,Ignacio Luque,Silvia Picossi

doi:10.3389/fmicb.2018.02260

Abstract

Filamentous cyanobacteria grow by intercalary cell division, which should involve distinct steps compared to those producing separate daughter cells. The N-terminal region of FtsZ is highly conserved in the clade of filamentous cyanobacteria capable of cell differentiation. A derivative of the model strain Anabaena sp. PCC 7120 expressing only an FtsZ lacking the amino acids 2–51 of the N-terminal peptide (ΔN-FtsZ) could not be segregated. Strain CSL110 expresses both ΔN-FtsZ, from the endogenous ftsZ gene promoter, and the native FtsZ from a synthetic regulated promoter. Under conditions of ΔN-FtsZ predominance, cells of strain CSL110 progressively enlarge, reflecting reduced cell division, and show instances of asymmetric cell division and aberrant Z-structures notably differing from the Z-ring formed by FtsZ in the wild type. In bacterial 2-hybrid assays FtsZ interacted with ΔN-FtsZ. However, ΔN-FtsZ-GFP appeared impaired for incorporation into Z-rings when expressed together with FtsZ. FtsZ, but not ΔN-FtsZ, interacted with the essential protein SepF. Both FtsZ and ΔN-FtsZ polymerize in vitro exhibiting comparable GTPase activities. However, filaments of FtsZ show a distinct curling forming toroids, whereas ΔN-FtsZ form thick bundles of straight filaments. Thus, the N-terminal FtsZ sequence appears to contribute to a distinct FtsZ polymerization mode that is essential for cell division and division plane location in Anabaena.

Highlights

In the vast majority of bacteria and archaea, FtsZ protein polymerization underneath the cytoplasmic membrane is the event initiating cell division
Results showed that (i) homologs were only present in the phylum Cyanobacteria; (ii) homologous sequences were always appended as an N-terminal region of FtsZ; and (iii) this sequence likely originated early during the diversification of cyanobacteria since it is observed in Pseudanabaena strains, which branch deeply in the phylum
FtsZ includes a significant N-terminal peptide preceding the conserved globular core characteristic of FtsZ proteins, and this region is highly conserved in the clade of filamentous heterocyst-forming strains

Summary

Introduction

In the vast majority of bacteria and archaea, FtsZ protein polymerization underneath the cytoplasmic membrane is the event initiating cell division. Besides its role at the initiation of divisome assembly, the Z-ring itself may contribute force for cytoplasmic membrane constriction during daughter cell separation (Li et al, 2007; Lutkenhaus et al, 2012; Coltharp et al, 2016). It has been proposed that directional movement of FtsZ filaments around the division ring by treadmilling guides the motion of septal cell wall synthesis enzymes, enabling correct envelope constriction and polar morphology (Bisson-Filho et al, 2017; Wagstaff et al, 2017; Yang et al, 2017). In recent years a number of new regulators of FtsZ assembly have been described in other bacteria, showing that a diversity of mechanisms for FtsZ-ring dynamics may operate outside the well-studied bacterial models (e.g., Thanbichler and Shapiro, 2006; Treuner-Lange et al, 2013; Fleurie et al, 2014; Bisson-Filho et al, 2015; Holecková et al, 2015)

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