Abstract

Magnetotactic bacteria are able to swim navigating along geomagnetic field lines. They synthesize ferromagnetic nanocrystals that are embedded in cytoplasmic membrane invaginations forming magnetosomes. Regularly aligned in the cytoplasm along cytoskeleton filaments, the magnetosome chain effectively forms a compass needle bestowing on bacteria their magnetotactic behaviour. A large genomic island, conserved among magnetotactic bacteria, contains the genes potentially involved in magnetosome formation. One of the genes, mamK has been described as encoding a prokaryotic actin-like protein which when it polymerizes forms in the cytoplasm filamentous structures that provide the scaffold for magnetosome alignment. Here, we have identified a series of genes highly similar to the mam genes in the genome of Magnetospirillum magneticum AMB-1. The newly annotated genes are clustered in a genomic islet distinct and distant from the known magnetosome genomic island and most probably acquired by lateral gene transfer rather than duplication. We focused on a mamK-like gene whose product shares 54.5% identity with the actin-like MamK. Filament bundles of polymerized MamK-like protein were observed in vitro with electron microscopy and in vivo in E. coli cells expressing MamK-like-Venus fusions by fluorescence microscopy. In addition, we demonstrate that mamK-like is transcribed in AMB-1 wild-type and ΔmamK mutant cells and that the actin-like filamentous structures observed in the ΔmamK strain are probably MamK-like polymers. Thus MamK-like is a new member of the prokaryotic actin-like family. This is the first evidence of a functional mam gene encoded outside the magnetosome genomic island.

Highlights

  • Magnetotactic bacteria (MTB) are a group of taxonomically, physiologically, and morphologically diverse prokaryotes with the ability to align along geomagnetic field lines [1,2,3]

  • We focused on the genome of M. magneticum AMB-1 and sought additional homologues of the mam genes in the entire genome

  • Using the MaGe interface for expert annotation of microbial genomes, we identified a new locus of approx. 22 kb outside the magnetosome island (MAI), containing seven ORFs similar to genes from the mamAB and mamCD operons

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Summary

Introduction

Magnetotactic bacteria (MTB) are a group of taxonomically, physiologically, and morphologically diverse prokaryotes with the ability to align along geomagnetic field lines [1,2,3]. The evolutionary advantage of possessing magnetosomes is possibly linked to the ability to efficiently navigate within zones of such sharp chemical gradients by simplifying a three-dimensional search for conditions of optimal oxygen concentration to a single dimension, northsouth. In the Magnetospirilla, the ‘compass needle’ is set parallel to the cell’s direction of movement, allowing passive alignment of the cell along geomagnetic field lines [5]. When MTB cells are disrupted, magnetosomes can be readily purified as closed vesicles encircling a single crystal by using magnets. The separation of functional membranes by magnetism elicits great interest in bio- and nanotechnology [6,7]

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