MamY is a membrane-bound protein that aligns magnetosomes and the motility axis of helical magnetotactic bacteria

Toro-Nahuelpan, Mauricio; Giacomelli, Giacomo; Raschdorf, Oliver; Borg, Sarah; Plitzko, Jürgen M.; Bramkamp, Marc; Schüler, Dirk; Müller, Frank-Dietrich

doi:10.1038/s41564-019-0512-8

Cited by 47 publications

(65 citation statements)

References 52 publications

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“…Several mam (magnetosome membrane) genes ( mamABEKMOPQI ) have been identified in all MTB genomes studied to date ( mamL is additionally present in all MTB that produce only magnetite) (Ji et al, 2017; Lefèvre, Trubitsyn, Abreu, Kolinko, Jogler, & de Almeida, 2013; Lin, Deng, et al, 2014). This suggests that these core genes control universal processes in all MTB, such as the biogenesis and assembly of the magnetosome membrane, Fe 2+ uptake, magnetite biomineralization, and chain assembly (Komeili, 2012; Toro‐Nahuelpan et al, 2019; Uebe & Schüler, 2016). MGC variability accounts for diverse crystal composition, shape, size, number, and intracellular organization of crystals and possibly results in species‐specific magnetite biomineralization in MTB.…”

Section: Discussionmentioning

confidence: 99%

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Menguy

Roberts

et al. 2020

JGR Biogeosciences

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Magnetite produced by magnetotactic bacteria (MTB) provides stable paleomagnetic signals because it occurs as natural single‐domain magnetic nanocrystals. MTB can also provide useful paleoenvironmental information because their crystal morphologies are associated with particular bacterial groups and the environments in which they live. However, identification of the fossil remains of MTB (i.e., magnetofossils) from ancient sediments or rocks is challenging because of their generally small sizes and because the growth, morphology, and chain assembly of magnetite within MTB are not well understood. Nanoscale characterization is, therefore, needed to understand magnetite biomineralization and to develop magnetofossils as biogeochemical proxies for paleoenvironmental reconstructions. Using advanced transmission electron microscopy, we investigated magnetite growth and chain arrangements within magnetotactic Deltaproteobacteria strain WYHR‐1, which reveals how the magnetite grows to form elongated, bullet‐shaped nanocrystals. Three crystal growth stages are recognized: (i) initial isotropic growth to produce nearly round ~20 nm particles, (ii) subsequent anisotropic growth along the [001] crystallographic direction to ~75 nm lengths and ~30–40 nm widths, and (iii) unidirectional growth along the [001] direction to ~180 nm lengths, with some growing to ~280 nm. Crystal growth and habit differ from that of magnetite produced by other known MTB strains, which indicates species‐specific biomineralization. These findings suggest that magnetite biomineralization might be much more diverse among MTB than previously thought. When characterized adequately at species level, magnetofossil crystallography, and apomorphic features are, therefore, likely to become useful proxies for ancient MTB taxonomic groups or species and for interpreting the environments in which they lived.

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Section: Discussionmentioning

confidence: 99%

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Menguy

Roberts

et al. 2020

JGR Biogeosciences

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“…1A). Recently, a further determinant named MamY was found to be required specifically for the positioning of magnetosome chains parallel to the motility axis of the cell (i.e., the direction of movement [4]) along regions of highest positive inner cell curvature (10). Deletion of mamY resulted in magnetosome chains located opposite to the geodetic motility axis (10) (as shown in Fig.…”

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confidence: 99%

“…1A). Based on the identification of MamY as a chain-positioning determinant, it was concluded that magnetosome chains in M. gryphiswaldense are localized along the cell's geodetic motility axis by a dedicated multipart magnetosome-specific cytoskeleton (i.e., the "magnetoskeleton," requiring the combined action of MamK, MamJ, and MamY) for most efficient magnetic navigation (10).…”

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confidence: 99%

“…Despite the detailed knowledge of the molecular determinants and mechanisms involved in magnetosome chain formation and positioning, the significance of the magnetoskeleton for magnetotaxis and the individual contributions of all key constituents in environmentally relevant magnetic fields have remained unstudied in a quantitative manner. Previous estimations of magnetic alignment (6,7,10,11) were mostly based on the C mag assay, an optical method based on the change in light scattering of the bacteria depending on cellular orientation (12). C mag measurements are a sensitive, fast, and simple method to analyze magnetic alignment.…”

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confidence: 99%

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Quantifying the Benefit of a Dedicated “Magnetoskeleton” in Bacterial Magnetotaxis by Live-Cell Motility Tracking and Soft Agar Swimming Assay

Pfeiffer

Schüler

2020

Appl Environ Microbiol

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The alphaproteobacterium Magnetospirillum gryphiswaldense has the intriguing ability to navigate within magnetic fields, a behavior named magnetotaxis, governed by the formation of magnetosomes, intracellular membrane-enveloped crystals of magnetite. Magnetosomes are aligned in chains along the cell’s motility axis by a dedicated multipart cytoskeleton (“magnetoskeleton”); however, precise estimates of its significance for magnetotaxis have not been reported. Here, we estimated the alignment of strains deficient in various magnetoskeletal constituents by live-cell motility tracking within defined magnetic fields ranging from 50 μT (reflecting the geomagnetic field) up to 400 μT. Motility tracking revealed that ΔmamY and ΔmamK strains (which assemble mispositioned and fragmented chains, respectively) are partially impaired in magnetotaxis, with approximately equal contributions of both proteins. This impairment was reflected by a required magnetic field strength of 200 μT to achieve a similar degree of alignment as for the wild-type strain in a 50-μT magnetic field. In contrast, the ΔmamJ strain, which predominantly forms clusters of magnetosomes, was only weakly aligned under any of the tested field conditions and could barely be distinguished from a nonmagnetic mutant. Most findings were corroborated by a soft agar swimming assay to analyze magnetotaxis based on the degree of distortion of swim halos formed in magnetic fields. Motility tracking further revealed that swimming speeds of M. gryphiswaldense are highest within the field strength equaling the geomagnetic field. In conclusion, magnetic properties and intracellular positioning of magnetosomes by a dedicated magnetoskeleton are required and optimized for bacterial magnetotaxis and most efficient locomotion within the geomagnetic field. IMPORTANCE In Magnetospirillum gryphiswaldense, magnetosomes are aligned in quasi-linear chains in a helical cell by a complex cytoskeletal network, including the actin-like MamK and adapter MamJ for magnetosome chain concatenation and segregation and MamY to position magnetosome chains along the shortest cellular axis of motility. Magnetosome chain positioning is assumed to be required for efficient magnetic navigation; however, the significance and contribution of all key constituents have not been quantified within defined and weak magnetic fields reflecting the geomagnetic field. Employing two different motility-based methods to consider the flagellum-mediated propulsion of cells, we depict individual benefits of all magnetoskeletal constituents for magnetotaxis. Whereas lack of mamJ resulted almost in an inability to align cells in weak magnetic fields, an approximately 4-fold-increased magnetic field strength was required to compensate for the loss of mamK or mamY. In summary, the magnetoskeleton and optimal positioning of magnetosome chains are required for efficient magnetotaxis.

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“…15-1. Very recently, MamY was demonstrated to determine the position of the magnetosome chain along the positive inner cell curvature of helically shaped MSR-1 cells (Toro-Nahuelpan et al, 2019). It, therefore, seems plausible that insufficient synthesis of MamY in Magnetospirillum sp.…”

Section: Discussionmentioning

confidence: 99%

Single‐step transfer of biosynthetic operons endows a non‐magnetotactic Magnetospirillum strain from wetland with magnetosome biosynthesis

Dziuba

Zwiener

Uebe

et al. 2020

Environmental Microbiology

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Summary The magnetotactic lifestyle represents one of the most complex traits found in many bacteria from aquatic environments and depends on magnetic organelles, the magnetosomes. Genetic transfer of magnetosome biosynthesis operons to a non‐magnetotactic bacterium has only been reported once so far, but it is unclear whether this may also occur in other recipients. Besides magnetotactic species from freshwater, the genus Magnetospirillum of the Alphaproteobacteria also comprises a number of strains lacking magnetosomes, which are abundant in diverse microbial communities. Their close phylogenetic interrelationships raise the question whether the non‐magnetotactic magnetospirilla may have the potential to (re)gain a magnetotactic lifestyle upon acquisition of magnetosome gene clusters. Here, we studied the transfer of magnetosome gene operons into several non‐magnetotactic environmental magnetospirilla. Single‐step transfer of a compact vector harbouring >30 major magnetosome genes from M. gryphiswaldense induced magnetosome biosynthesis in a Magnetospirillum strain from a constructed wetland. However, the resulting magnetic cellular alignment was insufficient for efficient magnetotaxis under conditions mimicking the weak geomagnetic field. Our work provides insights into possible evolutionary scenarios and potential limitations for the dissemination of magnetotaxis by horizontal gene transfer and expands the range of foreign recipients that can be genetically magnetized.

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MamY is a membrane-bound protein that aligns magnetosomes and the motility axis of helical magnetotactic bacteria

Cited by 47 publications

References 52 publications

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Quantifying the Benefit of a Dedicated “Magnetoskeleton” in Bacterial Magnetotaxis by Live-Cell Motility Tracking and Soft Agar Swimming Assay

Single‐step transfer of biosynthetic operons endows a non‐magnetotactic Magnetospirillum strain from wetland with magnetosome biosynthesis

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