Life with compass: diversity and biogeography of magnetotactic bacteria

Lin, Wei; Bazylinski, Dennis A.; Xiao, Tian; Wu, Long‐Fei; Pan, Yongxin

doi:10.1111/1462-2920.12313

Cited by 107 publications

(102 citation statements)

References 95 publications

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“…However, recent cultivation-independent analyses have revealed an unexpected diversity of MTB outside Proteobacteria (Kolinko et al, 2012;Lefèvre and Bazylinski, 2013;Lin et al, 2014). Among them, those belonging to the genus 'Candidatus Magnetobacterium' in the phylum Nitrospirae are of great interest (Garrity and Holt, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…Members of this genus, such as 'Candidatus M. bavaricum' (henceforth referred to as Mbav), have giant cell sizes (6-10 mm) and are capable of forming as many as 1000 bullet-shaped magnetite magnetosomes arranged into multiple bundles of chains in a single cell, which is different from Proteobacteria MTB (Spring et al, 1993). Originally discovered through electron microscope observation and ribosomal RNA gene sequencing (Vali et al, 1987;Spring et al, 1993), the Nitrospirae MTB are found to be widespread in aquatic environments and sometimes even account for a significant proportion (up to 30%) of microbial biomass in the microhabitats (Spring et al, 1993;Lin et al, 2014). Recent studies have suggested that these organisms may be capable of oxidizing sulfur (Spring and Bazylinski, 2006;Jogler et al, 2010), thus linking this genus to the key steps of iron and sulfur cycles in nature.…”

Section: Introductionmentioning

confidence: 99%

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Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

et al. 2014

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Magnetotactic bacteria (MTB) of the genus 'Candidatus Magnetobacterium' in phylum Nitrospirae are of great interest because of the formation of hundreds of bullet-shaped magnetite magnetosomes in multiple bundles of chains per cell. These bacteria are worldwide distributed in aquatic environments and have important roles in the biogeochemical cycles of iron and sulfur. However, except for a few short genomic fragments, no genome data are available for this ecologically important genus, and little is known about their metabolic capacity owing to the lack of pure cultures. Here we report the first draft genome sequence of 3.42 Mb from an uncultivated strain tentatively named 'Ca. Magnetobacterium casensis' isolated from Lake Miyun, China. The genome sequence indicates an autotrophic lifestyle using the Wood-Ljungdahl pathway for CO 2 fixation, which has not been described in any previously known MTB or Nitrospirae organisms. Pathways involved in the denitrification, sulfur oxidation and sulfate reduction have been predicted, indicating its considerable capacity for adaptation to variable geochemical conditions and roles in local biogeochemical cycles. Moreover, we have identified a complete magnetosome gene island containing mam, mad and a set of novel genes (named as man genes) putatively responsible for the formation of bullet-shaped magnetite magnetosomes and the arrangement of multiple magnetosome chains. This first comprehensive genomic analysis sheds light on the physiology, ecology and biomineralization of the poorly understood 'Ca. Magnetobacterium' genus.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

et al. 2014

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“…Magnetosomes are normally organized into chain-like structures to facilitate the navigation of MTB using Earth's magnetic field, a behavior known as magnetotaxis (2). Because of their ubiquitous distribution, MTB play key roles in global iron, nitrogen, sulfur, and carbon cycling (3). Magnetosome crystals can be preserved as magnetofossils after MTB die and lyse, and these crystals can be used as reliable biomarkers and are major contributors to sedimentary paleomagnetic records (4)(5)(6)(7).…”

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confidence: 99%

Origin of microbial biomineralization and magnetotaxis during the Archean

Lin

Paterson

Zhu

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Microbes that synthesize minerals, a process known as microbial biomineralization, contributed substantially to the evolution of current planetary environments through numerous important geochemical processes. Despite its geological significance, the origin and evolution of microbial biomineralization remain poorly understood. Through combined metagenomic and phylogenetic analyses of deep-branching magnetotactic bacteria from the Nitrospirae phylum, and using a Bayesian molecular clock-dating method, we show here that the gene cluster responsible for biomineralization of magnetosomes, and the arrangement of magnetosome chain(s) within cells, both originated before or near the Archean divergence between the Nitrospirae and Proteobacteria. This phylogenetic divergence occurred well before the Great Oxygenation Event. Magnetotaxis likely evolved due to environmental pressures conferring an evolutionary advantage to navigation via the geomagnetic field. Earth's dynamo must therefore have been sufficiently strong to sustain microbial magnetotaxis in the Archean, suggesting that magnetotaxis coevolved with the geodynamo over geological time.Archean | microbial biomineralization | magnetotaxis | magnetotactic bacteria | geodynamo

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“…The crystal sizes and shapes are highly regulated, and Ͼ10 magnetosomes typically align along the cell's long axis (8)(9)(10). Thus, the formation of magnetosomes confers a magnetic moment to the cells and allows them to migrate along oxygen gradients in an aquatic environment under the influence of the Earth's geomagnetic field (7).…”

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Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals

et al. 2016

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The magnetosome is an organelle specialized for inorganic magnetite crystal synthesis in magnetotactic bacteria. The complex mechanism of magnetosome formation is regulated by magnetosome proteins in a stepwise manner. Protein localization is a key step for magnetosome development; however, a global study of magnetosome protein localization remains to be conducted. Here, we comparatively analyzed the subcellular localization of a series of green fluorescent protein (GFP)-tagged magnetosome proteins. The protein localizations were categorized into 5 groups (short-length linear, middle-length linear, long-length linear, cell membrane, and intracellular dispersing), which were related to the protein functions. Mms6, which regulates magnetite crystal growth, localized along magnetosome chain structures under magnetite-forming (microaerobic) conditions but was dispersed in the cell under nonforming (aerobic) conditions. Correlative fluorescence and electron microscopy analyses revealed that Mms6 preferentially localized to magnetosomes enclosing magnetite crystals. We suggest that a highly organized spatial regulation mechanism controls magnetosome protein localization during magnetosome formation in magnetotactic bacteria. IMPORTANCEMagnetotactic bacteria synthesize magnetite (Fe 3 O 4 ) nanocrystals in a prokaryotic organelle called the magnetosome. This organelle is formed using various magnetosome proteins in multiple steps, including vesicle formation, magnetosome alignment, and magnetite crystal formation, to provide compartmentalized nanospaces for the regulation of iron concentrations and redox conditions, enabling the synthesis of a morphologically controlled magnetite crystal. Thus, to rationalize the complex organelle development, the localization of magnetosome proteins is considered to be highly regulated; however, the mechanisms remain largely unknown. Here, we performed comparative localization analysis of magnetosome proteins that revealed the presence of a spatial regulation mechanism within the linear structure of magnetosomes. This discovery provides evidence of a highly regulated protein localization mechanism for this bacterial organelle development. P rotein localization at appropriate positions within a cell is an essential mechanism for the effective performance of the diverse biological reactions that occur within the restricted intracellular area in both eukaryotes and prokaryotes. In various prokaryotes, intracellular compartments can be created to provide the domains required for highly specialized reactions. Whereas some of these compartments are completely proteinaceous (e.g., carboxysomes, metabolosomes, and ferritin) (1-3), others contain molecular components similar to those in cell membranes, including lipids and proteins (e.g., nucleoids, polyhydroxybutyrate, and spores) (4, 5). Such compartmentalized organelles are recognized to be formed within bacteria through multiple processes involving the spatial regulation of protein localization, but the details of this regulatory m...

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Life with compass: diversity and biogeography of magnetotactic bacteria

Cited by 107 publications

References 95 publications

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

Origin of microbial biomineralization and magnetotaxis during the Archean

Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals

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