Newly Isolated but Uncultivated Magnetotactic Bacterium of the Phylum Nitrospirae from Beijing, China

Abstract

Magnetotactic bacteria (MTB) in the phylum Nitrospirae synthesize up to hundreds of intracellular bullet-shaped magnetite magnetosomes. In the present study, a watermelon-shaped magnetotactic bacterium (designated MWB-1) from Lake Beihai in Beijing, China, was characterized. This uncultivated microbe was identified as a member of the phylum Nitrospirae and represents a novel phylogenetic lineage with >6% 16S rRNA gene sequence divergence from all currently described MTB. MWB-1 contained 200 to 300 intracellular bullet-shaped magnetite magnetosomes and showed a helical swimming trajectory under homogeneous magnetic fields; its magnetotactic velocity decreased with increasing field strength, and vice versa. A robust phylogenetic framework for MWB-1 and all currently known MTB in the phylum Nitrospirae was constructed utilizing maximumlikelihood and Bayesian algorithms, which yielded strong evidence that the Nitrospirae MTB could be divided into four well-supported groups. Considering its population densities in sediment and its high numbers of magnetosomes, MWB-1 was estimated to account for more than 10% of the natural remanent magnetization of the surface sediment. Taken together, the results of this study suggest that MTB in the phylum Nitrospirae are more diverse than previously realized and can make important contributions to the sedimentary magnetization in particular environments. Biomineralization of magnetic minerals has been discovered in a broad range of organisms, including birds, fishes, mollusks, insects, and microorganisms (23,53,55). A typical example of biomineralization is found in magnetotactic bacteria (MTB), a morphologically and phylogenetically diverse group of microorganisms that form special intracellular organelles, called magnetosomes (3, 5). Magnetosomes are membrane-enveloped, nanosized, high-purity crystals of iron oxide magnetite and/or iron sulfide greigite, usually arranged into one or more linear chains (21). These specific organelles help MTB to sense and swim along the earth's magnetic field, a behavior known as magnetotaxis (8). In conjunction with aerotaxis and chemotaxis, magnetotaxis facilitates the location of MTB to their favorable positions in vertical chemical gradients in the oxic-anoxic transition zone (OATZ) (11,40). The ubiquity and abundance of MTB near the OATZ suggest their potentially important roles in the geochemical cycling of iron and sulfur in nature (48). Molecular approaches based on 16S rRNA gene sequencing have provided evidence for the phylogenetic heterogeneity of MTB. Most discovered MTB are affiliated with the Alphaproteobacteria, but MTB belonging to the Gammaproteobacteria, the Deltaproteobacteria, and Nitrospirae have also been described (2, 28).One of the most intriguing examples of MTB is "Candidatus Magnetobacterium bavaricum," a magnetite-producing MTB within the deep-branching bacterial phylum Nitrospirae that was first discovered in Lake Chiemsee in Upper Bavaria, Germany (49, 54). "Ca. Magnetobacterium bavaricum" is a large, rod-shaped bact...

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

“…PCR and fluorescence in situ hybridization 16S rRNA gene was amplified using the universal bacterial primers 27F (5 0 -AGAGTTTGATCCTGGCT CAG-3 0 ) and 1492R (5 0 -GGTTACCTTGTTACGACTT-3 0 ; Lin et al, 2012). After gel purification, the PCR product was cloned into the pMD19-T vector to construct two clone libraries.…”

“…Fluorescence in situ hybridization was carried out as described previously (Lin et al, 2012). A Cy3-labeled-specific probe for the genus 'Ca.…”

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

“…Magnetoovum mohavensis," strain MWB-1, was isolated from Lake Beihai in Beijing, China, and shares 95% 16S rRNA gene sequence identity with "Ca. Magnetoovum mohavensis" (147). The watermelon-shaped strain MWB-1 appears to account for Ͼ10% of the natural remanent magnetization of the surface sediment of Lake Beihai (147).…”

“…Magnetobacterium bavaricum" and "Ca. Magnetoovum mohavensis," isolated from freshwater lakes in Beijing, China, were also recently described (146,147). All known magnetotactic Nitrospirae biomineralize bullet-shaped crystals of magnetite ( Fig.…”

Characterization of uncultured giant rod-shaped magnetotactic Gammaproteobacteria from a freshwater pond in Kanazawa, Japan

“…These MTB were similar in length (mean 10.07±1.87 mm) to GRS-1, but they were much narrower (mean width of 3.51±0.49 mm). Characterization of giant rod-shaped MTB MTB, which swim at speeds greater than 100 mm s 21 (Lefèvre et al, 2010;Lin et al, 2012). When viewed in the SEM, the oval shape of GRS-1 cells was discernible (Fig.…”