Metagenomic Analysis Reveals Unexpected Subgenomic Diversity of Magnetotactic Bacteria within the Phylum
            <i>Nitrospirae</i>

Lin, Wei; Jogler, Christian; Schüler, Dirk; Pan, Yongxin

doi:10.1128/aem.01476-10

Cited by 42 publications

(53 citation statements)

References 23 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…S7). The G+C content of 49.7% is within the range of 46.9-50.2% as determined for metagenomic fosmid clones containing phylogenetic marker genes (16S rRNA) from Mbav-like MTB (21,30), but differs significantly from the related T. yellowstonii (34%), although it is well below the range of percentage of G+C found in MTB thus far (54.8-65.1%) (8). Out of the 34 identified genes, 14 encode hypothetical proteins, and 2 share no similarity to the NCBI database (Table S1).…”

Section: Resultsmentioning

confidence: 99%

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Jogler

Wanner

Kolinko

et al. 2010

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

Self Cite

107

172

View full text Add to dashboard Cite

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.M agnetotactic bacteria (MTB) are widespread aquatic microorganisms that use unique intracellular organelles called magnetosomes to navigate along the earth's magnetic field while searching for growth-favoring microoxic zones within stratified sediments. In strains of Magnetospirillum, it was shown that magnetosomes consist of magnetite (Fe 3 O 4 ) crystals enclosed by a dedicated phospholipid membrane. The magnetosome membrane (MM) contains a specific set of proteins (1-3), which direct the biomineralization of highly ordered crystals along actin-like cytoskeletal filaments that control the assembly and intracellular positioning of a linear magnetosome chain (4-7). Synthesis of magnetosomes has recently emerged as a model for prokaryotic organelle formation and biomineralization (8-11). The trait of magnetotaxis is widely spread among Proteobacteria including members from the α-, δ-and γ-subdivisions, as well as uncultivated species from the deep branching Nitrospira phylum (8). The presence of MTB within unrelated lines of various phylogenetic groups, as well as their stunning diversity with respect to magnetosome shape, composition, and intracellular organization lead to speculations of whether the evolutionary origin of magnetota...

show abstract

Section: Resultsmentioning

confidence: 99%

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Jogler

Wanner

Kolinko

et al. 2010

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

Self Cite

107

172

View full text Add to dashboard Cite

show abstract

“…A Cy3-labeled-specific probe for the genus 'Ca. Magnetobacterium' (5 0 -GCCATCCCCTCGCTTACT-3 0 ; named BaP in this study) (Spring et al, 1993;Lin et al, 2011) and the 6-carboxyfluorescein-labeled bacterial universal probe EUB338 (5 0 -GCTGCCTCCCGTAGGAGT-3 0 ; Amann et al, 1990) were used for hybridization.…”

Section: Methodsmentioning

confidence: 99%

“…These MTB were magnetically collected and purified through the 'MTB trap' method Table 1). The GC content of the assembled genome is 48.9%, within the range of 45.1-50.2% as determined from the metagenomic fosmids of the Nitrospirae MTB Lin et al, 2011). The draft genome contains 3140 predicted genes, 40 tRNAs and one complete rRNA gene operon ( Table 1) that provides a wealth of genomic information valuable for understanding the biology of this poorly understood magnetotactic lineage.…”

Section: General Genomic Featuresmentioning

confidence: 99%

“…Magnetobacterium' genus, which has recently been identified from Lake Miyun near Beijing, China Li et al, 2010;Lin et al, 2011). This bacterium is morphologically similar to Mbav and contains hundreds bullet-shaped magnetite magnetosomes that are arranged into multiple bundles of chains Lin et al, 2011; Figure 1). The draft genome sequence retrieved here has allowed us to gain novel insights into the metabolism and physiological ecology of this poorly understood genus.…”

Section: Introductionmentioning

confidence: 99%

“…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. However, except for a few short genomic fragments (Jogler et al, 2010;Jogler et al, 2011;Lin et al, 2011), very little genetic data of this genus are available owing to their unculturability. Consequently, knowledge of their trophic strategy, physiology and intracellular biomineralization remains very limited.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

et al. 2014

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Magnetotaxis in Prokaryotes

Lefèvre¹,

Frankel²,

Bazylinski³

2011

Encyclopedia of Life Sciences

View full text Add to dashboard Cite

Magnetotaxis refers to the behaviour of some motile, aquatic, bacteria that orient and swim along magnetic field lines. These microorganisms, called magnetotactic bacteria (MTB), contain intracellular structures known as magnetosomes, which are nano‐sized, magnetic, iron‐mineral crystals, each enveloped by a biological (phospholipid bilayer) membrane. Magnetosomes are usually arranged in chains within the cell, providing it with a permanent magnetic dipole moment that facilitates location and retention in the cell's preferred habitat at or below the oxic–anoxic interface in the water column or sediment. Although all MTB are motile by means of flagella and have a cell wall structure characteristic of Gram‐negative bacteria, their diversity is reflected by the large number of different morphotypes found in environmental samples of water or sediment, and by phylogenetic analysis of both cultured and uncultured organisms. Key Concepts: Prokaryotes (bacteria), like eukaryotes, internally compartmentalise and contain organelles. The prokaryotic flagellum rotates clockwise and counter clockwise thereby propelling the cell during swimming. Magnetotaxis is bacterial motility directed by a magnetic field. Magnetotactic bacteria contain intracellular, nano‐scale, membrane‐enveloped, magnetic iron‐mineral crystals called magnetosomes. Magnetosomes impart a permanent magnetic dipole moment to cells of magnetotactic bacteria causing them to behave as miniature, motile, compass needles. Magnetotaxis works in conjunction with aerotaxis to increase energy transduction in magnetotactic bacteria. Genes for magnetosome formation are clustered in a region of the genomes of magnetotactic bacteria known as a magnetosome gene or genomic island. Magnetotactic bacteria are important in the cycling of a number of important elements including carbon, iron, nitrogen and sulfur.

show abstract

Metagenomic Analysis Reveals Unexpected Subgenomic Diversity of Magnetotactic Bacteria within the Phylum Nitrospirae

Cited by 42 publications

References 23 publications

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branchingNitrospiraphylum

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

Magnetotaxis in Prokaryotes

Contact Info

Product

Resources

About