Phylogenetic and Structural Identification of a Novel Magnetotactic Deltaproteobacteria Strain, WYHR-1, from a Freshwater Lake.

Abstract

Magnetotactic bacteria (MTB) are phylogenetically diverse prokaryotes that are able to biomineralize intracellular, magnetic chains of magnetite or greigite nanocrystals called magnetosomes. Simultaneous characterization of MTB phylogeny and biomineralization is crucial but challenging because most MTB are extremely difficult to culture. We identify a large rod, bean-like MTB (tentatively named WYHR-1) from freshwater sediments of Weiyang Lake, Xi'an, China, using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Phylogenetic analysis of 16S rRNA gene sequences indicates that WYHR-1 is a novel genus from the Deltaproteobacteria class. Transmission electron microscope observations reveal that WYHR-1 cells contain tens of magnetite magnetosomes that are organized into a single chain bundle along the cell long axis. Mature WYHR-1 magnetosomes are bullet-shaped, straight, and elongated along the [001] direction, with a large flat end terminated by a {100} face at the base and a conical top. This crystal morphology is distinctively different from bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum. This indicates that WYHR-1 may have a different crystal growth process and mechanism from other species, which results from species-specific magnetosome biomineralization in MTB.IMPORTANCE Magnetotactic bacteria (MTB) represent a model system for understanding biomineralization and are also studied intensively in biogeomagnetic and paleomagnetic research. However, many uncultured MTB strains have not been identified phylogenetically or investigated structurally at the single-cell level, which limits comprehensive understanding of MTB diversity and their role in biomineralization. We have identified a novel MTB strain, WYHR-1, from a freshwater lake using a coupled fluorescence and scanning electron microscopy approach at the single-cell scale. Our analyses further indicate that strain WYHR-1 represents a novel genus from the Deltaproteobacteria class. In contrast to bullet-shaped magnetosomes produced by other MTB in the Deltaproteobacteria class and the Nitrospirae phylum, WYHR-1 magnetosomes are bullet-shaped, straight, and highly elongated along the [001] direction, are terminated by a large {100} face at their base, and have a conical top. Our findings imply that, consistent with phylogenetic diversity of MTB, bullet-shaped magnetosomes have diverse crystal habits and growth patterns.