Novel species and expanded distribution of ellipsoidal multicellular magnetotactic prokaryotes.

Multicellular magnetotactic prokaryotes (MMPs) are a peculiar group of magnetotactic bacteria, each comprising approximately 10-100 cells of the same phylotype. Two morphotypes of MMP have been identified, including several species of globally distributed spherical mulberry-like MMPs (s-MMPs), and two species of ellipsoidal pineapple-like MMPs (e-MMPs) from China (Qingdao and Rongcheng cities). We recently collected e-MMPs from Mediterranean Sea sediments (Six-Fours-les-Plages) and Drummond Island, in the South China Sea. Phylogenetic analysis revealed that the MMPs from Six-Fours-les-Plages and the previously reported e-MMP Candidatus Magnetananas rongchenensis have 98.5% sequence identity and are the same species, while the MMPs from Drummond Island appear to be a novel species, having > 7.1% sequence divergence from the most closely related e-MMP, Candidatus Magnetananas tsingtaoensis. Identification of the novel species expands the distribution of e-MMPs to Tropical Zone. Comparison of nine physical and chemical parameters revealed that sand grain size and the content of inorganic nitrogen (nitrate, ammonium and nitrite) in the sediments from Rongcheng City and Six-Fours-les-Plages were similar, and lower than found for sediments from the other two sampling sites. The results of the study reveal broad diversity and wide distribution of e-MMPs.

Temporal distributions and environmental adaptations of two types of multicellular magnetotactic prokaryote in the sediments of Lake Yuehu, China.

Two morphotypes (spherical and ellipsoidal) of multicellular magnetotactic prokaryotes (MMPs) have been reported from the sediments of Lake Yuehu, China. Here, their temporal distributions and their relationships with biogeochemical parameters are studied. Samples were collected at approximately 2-week intervals from two sites (A and B) during the period September 2012 to December 2013. The abundance of MMPs was high in summer and autumn, but low in winter and spring. Furthermore, the peaks in the numbers of the two types of MMPs were sequential, with the highest concentration of the spherical MMPs occurring prior to that of the ellipsoidal MMPs. This may be related to different optimal growth temperatures for the two types. Although the two types of MMP coexisted at both sites, their numbers were different; at most times, spherical MMPs dominated at site A, whereas ellipsoidal MMPs dominated at site B. Geochemical analysis revealed that the environmental conditions at site A varied more than at site B. Compared with the widely distributed spherical MMPs, ellipsoidal MMPs seemed to prefer more stable habitats. This is the first report of the temporal distribution of ellipsoidal MMPs in sediments, suggesting that their environmental adaptations differ from those of spherical MMPs.

A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China.

Two morphotypes of multicellular magnetotactic prokaryotes (MMPs) have been identified: spherical (several species) and ellipsoidal (previously one species). Here, we report novel ellipsoidal MMPs that are ∼ 10 × 8 µm in size, and composed of about 86 cells arranged in six to eight interlaced circles. Each MMP was composed of cells that synthesized either bullet-shaped magnetite magnetosomes alone, or both bullet-shaped magnetite and rectangular greigite magnetosomes. They showed north-seeking magnetotaxis, ping-pong motility and negative phototaxis at a velocity up to 300 µm s(-1) . During reproduction, they divided along either their long- or short-body axes. For genetic analysis, we sorted the ellipsoidal MMPs with micromanipulation and amplified their genomes using multiple displacement amplification. We sequenced the 16S rRNA gene and found 6.9% sequence divergence from that of ellipsoidal MMPs, Candidatus Magnetananas tsingtaoensis and > 8.3% divergence from those of spherical MMPs. Therefore, the novel MMPs belong to different species and genus compared with the currently known ellipsoidal and spherical MMPs respectively. The novel MMPs display a morphological cell differentiation, implying a potential division of labour. These findings provide new insights into the diversity of MMPs in general, and contribute to our understanding of the evolution of multicellularity among prokaryotes.

Characterization and phylogenetic identification of a species of spherical multicellular magnetotactic prokaryotes that produces both magnetite and greigite crystals.

Magnetotactic bacteria (MTB) are a group of Gram-negative bacteria synthesizing magnetic crystals that allow them aligning along magnetic field lines. They have diverse morphologies including cocci, rods, vibrio, spirilla, and multicellular magnetotactic prokaryotes (MMPs). MMPs are composed of 10-57 cells with peritrichous flagella on their outer surfaces and swim as an entire unit. Here, we describe a species of spherical MMPs isolated from intertidal sediments of Lake Yuehu (Yellow Sea, China). They were mainly found in the subsurface layer of gray-black sediments. Microscopy revealed that these spherical MMPs were 5.6 ± 0.9 µm in diameter and composed of approximately 16-32 ovoid cells with a helical arrangement and peritrichous flagellation. High-resolution transmission electron microscopy showed that the MMPs contained both bullet-shaped magnetite and irregular greigite magnetosomes that were arranged in chains or clusters. These MMPs displayed typical escape motility and negative phototaxis. The 16S rRNA genes of micromanipulation-purified spherical MMPs were cloned and sequenced. Phylogenetic analysis revealed that the MMP species was affiliated with Deltaproteobacteria and displayed >2.8% sequence divergence with respect to previously reported MMPs. This is the first phylogenetic identification of a spherical MMP that produces both magnetite and greigite magnetosomes.

Novel rod-shaped magnetotactic bacteria belonging to the class Alphaproteobacteria.

Novel large, rod-shaped magnetotactic bacteria (MTB) were discovered in intertidal sediments of the Yellow Sea, China. They biomineralized more than 300 rectangular magnetite magnetosomes per cell. Phylogenetic analysis based on the 16S rRNA gene sequence revealed that they are affiliated with the Alphaproteobacteria and may represent a new genus of MTB.

Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone.

A combination of microscopic, molecular and biogeochemical methods was used to study the structure, phylogenetics and vertical distribution of spherical multicellular magnetotactic prokaryotes (MMPs) of intertidal sediments in the Yellow Sea. These MMPs were 5.5 µm in diameter and composed of approximately 15-30 cells. They synthesized bullet-shaped magnetites in chains or clusters. Phylogenetic analysis of 16S rRNA gene sequences suggested that these MMPs represent a novel species affiliated to the Deltaproteobacteria. To study their vertical distribution and the relationship to geochemical parameters, sediment cores were collected after the redox potential was measured in situ. The sediments were composed of yellow, grey and black layers from the surface to depth. The spherical MMPs were concentrated near the grey-black layer transition at a depth of 8-12 cm, while coccoid-shaped magnetotactic bacteria near the yellow-grey layer transition at a depth of 3-5 cm. The intertidal MMPs showed a deeper distribution at more reduced environments than coccoid-shaped magnetotactic bacteria, and MMPs in lagoon sediments. Additionally the MMPs were concentrated significantly in layers with high proportion of fine sand and total organic carbon, rich in leachable iron but poor in nitrate. These results show an adaptation of spherical MMPs to the peculiar intertidal sediment habitat.

Two genera of magnetococci with bean-like morphology from intertidal sediments of the Yellow Sea, China.

Magnetotactic bacteria have the unique capacity of being able to swim along geomagnetic field lines. They are Gram-negative bacteria with diverse morphologies and variable phylogenetic relatedness. Here, we describe a group of uncultivated marine magnetococci collected from intertidal sediments of Huiquan Bay in the Yellow Sea. They were coccoid-ovoid in morphology, with an average size of 2.8 ± 0.3 µm by 2.0 ± 0.2 µm. Differential interference contrast microscopy, fluorescence microscopy, and transmission electron microscopy revealed that each cell was apparently composed of two hemispheres. The cells synthesized iron oxide-type magnetosomes that clustered on one side of the cell at the interface between the two hemispheres. In some cells two chains of magnetosomes were observed across the interface. Each cell had two bundles of flagella enveloped in a sheath and displayed north-seeking helical motion. Two 16S rRNA gene sequences having 91.8% identity were obtained, and their authenticity was confirmed by fluorescence in situ hybridization. Phylogenetic analysis revealed that the magnetococci are affiliated with the Alphaproteobacteria and are most closely related to two uncultured magnetococci with sequence identities of 92.7% and 92.4%, respectively. Because they display a >7% sequence divergence to all bacteria reported, the bean-like magnetococci may represent two novel genera.

A novel genus of multicellular magnetotactic prokaryotes from the Yellow Sea.

Multicellular magnetotactic prokaryotes (MMPs) are a group of magnetotactic microorganisms composed of 10-40 Gram-negative cells. Currently, all the identified MMPs show a spherical morphology and synthesize mainly iron sulfide magnetosomes. In this study, we report a novel genus of MMPs with peculiar ellipsoidal morphology and iron oxide magnetosomes, which were discovered in intertidal sediment of the Yellow Sea in China. Optical and fluorescence microscopy revealed that this organism was ~10 × 8 µm in size and composed of ~40 cells enveloped by an outer layer. Scanning electron microscopy showed that the cells were arranged in 4-6 interlaced circles. Bullet-shaped magnetite magnetosomes were organized in chains roughly parallel to the long axis of the ellipsoidal MMPs when analysed by transmission electron microscopy. These MMPs displayed special escape motility, i.e. swimming rapidly from the edge to the centre of the droplet and then slowly back to the edge. In addition, they exhibited negative phototaxis. Light microscopy observations showed that the ellipsoidal MMPs reproduced by division along the body long axis. Both analysis of 16S rRNA gene sequence and fluorescence in situ hybridization revealed the ellipsoidal MMPs as a new genus of the Deltaproteobacteria. In summary, this novel genus of MMPs exhibit unique morphology, peculiar division process and distinct phylogenetic affiliation compared with the other MMPs.