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Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum - PubMed

  • ️Sat Jan 01 2011

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum

Christian Jogler et al. Proc Natl Acad Sci U S A. 2011.

Abstract

Magnetotactic bacteria (MTB) are a phylogenetically diverse group which uses intracellular membrane-enclosed magnetite crystals called magnetosomes for navigation in their aquatic habitats. Although synthesis of these prokaryotic organelles is of broad interdisciplinary interest, its genetic analysis has been restricted to a few closely related members of the Proteobacteria, in which essential functions required for magnetosome formation are encoded within a large genomic magnetosome island. However, because of the lack of cultivated representatives from other phyla, it is unknown whether the evolutionary origin of magnetotaxis is monophyletic, and it has been questioned whether homologous mechanisms and structures are present in unrelated MTB. Here, we present the analysis of the uncultivated "Candidatus Magnetobacterium bavaricum" from the deep branching Nitrospira phylum by combining micromanipulation and whole genome amplification (WGA) with metagenomics. Target-specific sequences obtained by WGA of cells, which were magnetically collected and individually sorted from sediment samples, were used for PCR screening of metagenomic libraries. This led to the identification of a genomic cluster containing several putative magnetosome genes with homology to those in Proteobacteria. A variety of advanced electron microscopic imaging tools revealed a complex cell envelope and an intricate magnetosome architecture. The presence of magnetosome membranes as well as cytoskeletal magnetosome filaments suggests a similar mechanism of magnetosome formation in "Cand. M. bavaricum" as in Proteobacteria. Altogether, our findings suggest a monophyletic origin of magnetotaxis, and relevant genes were likely transferred horizontally between Proteobacteria and representatives of the Nitrospira phylum.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Scanning (SEM) and transmission electron (TEM) micrographs of “Candidatus M. bavaricum” cells (Mbav). (A) SEM micrograph of Mbav by simultaneous detection of secondary (blue) and backscattered electrons (red). Chains of magnetite crystals are visible (red). (B–D) TEM microcraphs of ultrathin sections of high-pressure frozen and freeze-substituted cells showing the multilayered cell boundary (B, framed area). CM, cytoplasmic membrane; OM, outer membrane; PG, peptidoglycan; OL1, inner part of outer layer; OL2, outer part of outer layer; asterisks, ridges or papillae of periplasmic space. (E) FIB section showing a network of extensions of ridges. (F and G) TEM and SEM of conventionally fixed samples (Fl, flagella). (H) High-resolution SEM of a high-pressure frozen, cryofractured, and frozen hydrated Mbav cell. Solid circle, magnetosome crystals; dotted circle, empty magnetosome membrane vesicles.

Fig. 2.
Fig. 2.

TEM and SEM micrographs of Mbav magnetosome chains (see

Fig. S3

for an enlarged version at higher resolution). (A) SEM microcraph of a cryofractured cell (after chemical fixation) showing two bundles of magnetosome strands. (B and C) TEM ultrathin sections of high-pressure frozen and freeze-substituted cells showing strands of magnetosomes aligned parallel to a tubular filamentous structure (asterisk, framed area; MM, magnetosome membrane). (D and E) Cryo-SEM (frozen hydrated) of tangential (D) and cross-fractured (E) cells of Mbav (rectangular frame, magnetosomes aligned along MF; solid circles, magnetosomes crystals; dotted circle, empty MM vesicles). (F and G) SEM of focused ion beam (FIB) sections (F), and high-pressure frozen and freeze-substituted (G) Mbav cells. Circles indicate several rosette-like magnetosome bundles. Different micrographs in G represent selected sections from FIB-milling series (every 10th section is shown from left to right). Each section has a thickness of 8 nm.

Fig. 3.
Fig. 3.

Molecular organization of sections from putative magnetosome islands of Mbav and selected other MTB (Mbav, Candidatus M. bavaricum; MV-1, magnetic vibrio; Fos001+002, metagenomic MTB clones; MSR-1, Magnetospirillum gryphiswaldense; MC-1, magnetic coccus; RS-1, Desulfovibrio magneticus). The black arrow on Top indicates the extension of a putative magnetosome operon in Mbav. Different colored arrows indicate characteristic features of proteins encoded by known magnetosome genes, whereas equivalent genes are connected by stripes of various shadings, which indicate different degrees of identity (id) as calculated from ClustalW alignments of encoded proteins. Alignments were generated with TRAPPIST, a Python-based toolbox for alignment, analysis, and visualization of genomes or genome segments.

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