The FtsZ-Like Protein FtsZm of Magnetospirillum gryphiswaldense Likely Interacts with Its Generic Homolog and Is Required for Biomineralization under Nitrate Deprivation

Abstract

dMidcell selection, septum formation, and cytokinesis in most bacteria are orchestrated by the eukaryotic tubulin homolog FtsZ. The alphaproteobacterium Magnetospirillum gryphiswaldense (MSR-1) septates asymmetrically, and cytokinesis is linked to splitting and segregation of an intracellular chain of membrane-enveloped magnetite crystals (magnetosomes). In addition to a generic, full-length ftsZ gene, MSR-1 contains a truncated ftsZ homolog (ftsZm) which is located adjacent to genes controlling biomineralization and magnetosome chain formation. We analyzed the role of FtsZm in cell division and biomineralization together with the full-length MSR-1 FtsZ protein. Our results indicate that loss of FtsZm has a strong effect on microoxic magnetite biomineralization which, however, could be rescued by the presence of nitrate in the medium. Fluorescence microscopy revealed that FtsZm-mCherry does not colocalize with the magnetosome-related proteins MamC and MamK but is confined to asymmetric spots at midcell and at the cell pole, coinciding with the FtsZ protein position. In Escherichia coli, both FtsZ homologs form distinct structures but colocalize when coexpressed, suggesting an FtsZdependent recruitment of FtsZm. In vitro analyses indicate that FtsZm is able to interact with the FtsZ protein. Together, our data suggest that FtsZm shares key features with its full-length homolog but is involved in redox control for magnetite crystallization. Magnetotactic bacteria (MTB) produce magnetosomes to navigate along Earth's magnetic field lines toward growth-favoring microoxic environments. Magnetosomes consist of nanometer-sized membrane-enveloped magnetite crystals and have recently emerged as a model system to study formation of prokaryotic organelles (1). In the alphaproteobacterium Magnetospirillum gryphiswaldense MSR-1 (in the following, referred to as MSR-1) and related magnetospirilla, the intracellular organelles are attached to a filamentous cytoskeletal structure formed by the actinlike MamK protein (2, 3, 4) which assembles magnetosomes into a cohesive chain (5). This magnetosome chain generates a magnetic moment which aligns the cell in external magnetic fields. In order to be cleaved evenly during cytokinesis and to be equipartitioned to daughter cells, the magnetosome chain is positioned at midcell. After cytokinesis, daughter chains are translocated to midcell again, suggesting that chain separation and relocalization are coordinated with the cell cycle.A crucial factor for midcell determination and septum formation in most bacteria is the conserved tubulin homolog FtsZ. FtsZ monomers assemble in a GTP-dependent manner to form protofilaments that align into higher-ordered structures by lateral selfinteraction assisted by accessory proteins. The FtsZ polymers are membrane tethered by C-terminal interaction with FtsA and build ring-or arc-like structures at future division sites (6). These FtsZ assemblies recruit further cell division proteins to finally build the divisome complex (7,8). Several factors have ...

The Terminal Oxidase cbb 3 Functions in Redox Control of Magnetite Biomineralization in Magnetospirillum gryphiswaldense

“…However, an optimal redox state (i.e., balanced ratio of Fe 2ϩ /Fe 3ϩ ) seems to be very important for microaerobic biomineralization of the mixed-valence iron oxide magnetite [Fe(II)Fe(III) 2 O 4 ], especially in the presence of nitrate, and some other factors involved in magnetite biosynthesis are also likely affected by the loss of cbb 3 oxidase. For example, several proteins encoded within the genomic magnetosome island, such as MamX, MamZ, and the FtsZ-like protein FtsZm, displayed different defects in magnetosome formation depending on the presence and absence of nitrate (37,38). MTB contain a unique set of redox-active magnetosome-associated proteins, including MamP, MamX, MamE, and MamT, which share a novel configuration of two close CXXCH hemebinding motifs, the magnetochrome domain (37,39,40).…”

From invagination to navigation: The story of magnetosome-associated proteins in magnetotactic bacteria

“…Deletion of ftsZm had no significant impact on cell growth, which suggests that it does not have the cell‐division function of other bacterial FtsZ proteins . Conversely, overexpression of FtsZm interfered in cell division similarly to other FtsZ proteins . Studies showed that ftsZm deletion caused changes in magnetite size and morphology only when cells grew in the presence of ammonia instead of nitrate .…”

“…FtsZ are structural, bacterial tubulin‐like cell‐division proteins that assembles into ring‐like structures in a GTP‐dependent manner in the dividing cell septum . In at least three Magnetospirillum species, there is a second copy of a conserved ftsZ ‐like gene located in the mamXY operon that encodes FtsZm, a truncated C‐terminal FtsZ protein . FtsZm's structural model consists of a GTP binding site in the N‐terminal domain (NTD) and a CTD, that is essential for FtsZ polymerization and interactions with other proteins .…”

“…Mam and Mms proteins can be classified approximately into several groups according to their roles during magnetosome formation processes, such as membrane invagination, protein sorting, magnetosome alignment into chains, biomineralization, and the control of mineral crystal shape and size . Here, by describing the known data regarding Mam and Mms proteins and focusing on their role (Table ), we present the process of magnetosome formation.…”

Magnetita biomimética mediada por proteínas del magnetosoma vs. magnetita del meteorito ALH84001: ¿Son ambas comparables?

“…28 (2016) 41-63 49 (Murat et al, 2010). The FtsZ-like protein is a truncated homologous of the FtsZ protein (Ding et al, 2010), but unlike the full length FtsZ, which is still functional in in cell division, FtsZ-like is involved in redox control of magnetite crystallization (Müller et al, 2014) and crystal size and shape (Ding et al, 2010). MamG, MamF, MamD and MamC are all encoded in the mamGFDC operon.…”