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Constant Flux of Spatial Niche Partitioning through High-Resolution Sampling of Magnetotactic Bacteria.

ABSTRACT: Magnetotactic bacteria (MTB) swim along magnetic field lines in water. They are found in aquatic habitats throughout the world, yet knowledge of their spatial and temporal distribution remains limited. To help remedy this, we took MTB-bearing sediment from a natural pond, mixed the thoroughly homogenized sediment into two replicate aquaria, and then counted three dominant MTB morphotypes (coccus, spirillum, and rod-shaped MTB cells) at a high spatiotemporal sampling resolution: 36 discrete points in replicate aquaria were sampled every ∼30 days over 198 days. Population centers of the MTB coccus and MTB spirillum morphotypes moved in continual flux, yet they consistently inhabited separate locations, displaying significant anticorrelation. Rod-shaped MTB were initially concentrated toward the northern end of the aquaria, but at the end of the experiment, they were most densely populated toward the south. The finding that the total number of MTB cells increased over time during the experiment argues that population reorganization arose from relative changes in cell division and death and not from migration. The maximum net growth rates were 10, 3, and 1 doublings day^-1 and average net growth rates were 0.24, 0.11, and 0.02 doublings day^-1 for MTB cocci, MTB spirilla, and rod-shaped MTB, respectively; minimum growth rates for all three morphotypes were -0.03 doublings day^-1 Our results suggest that MTB cocci and MTB spirilla occupy distinctly different niches: their horizontal positioning in sediment is anticorrelated and under constant flux.IMPORTANCE Little is known about the horizontal distribution of magnetotactic bacteria in sediment or how the distribution changes over time. We therefore measured three dominant magnetotactic bacterium morphotypes at 36 places in two replicate aquaria each month for 7 months. We found that the spatial positioning of population centers changed over time and that the two most abundant morphotypes (MTB cocci and MTB spirilla) occupied distinctly different niches in the aquaria. Maximum and average growth and death rates were quantified for each of the three morphotypes based on 72 sites that were measured six times. The findings provided novel insight into the differential behavior of noncultured magnetotactic bacteria.

SUBMITTER: He K

PROVIDER: S-EPMC5626982 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Magnetotactic bacteria (MTB) form intracellular chain-assembled nanocrystals of magnetite or greigite termed magnetosomes. The characterization of magnetosome crystals requires electron microscopy due to their nanoscopic sizes. However, electron microscopy does not provide phylogenetic information for MTB. We have developed a strategy for the simultaneous and rapid phylogenetic and biomineralogical characterization of uncultured MTB at the single-cell level. It consists of four steps: (i) enrichment of MTB cells from an environmental sample, (ii) 16S rRNA gene sequencing of MTB, and (iii) fluorescence in situ hybridization analyses coordinated with (iv) transmission or scanning electron microscopy of the probe-hybridized cells. The application of this strategy identified a magnetotactic Gammaproteobacteria strain, SHHR-1, from brackish sediments collected from the Shihe River estuary in Qinhuangdao City, China. SHHR-1 magnetosomes are elongated prismatic magnetites which can be idealized as hexagonal prisms. Taxonomic groups of uncultured MTB were also identified in freshwater sediments from Lake Miyun in northern Beijing via this novel coordinated fluorescence and scanning electron microscopy method based on four group-specific rRNA-targeted probes. Our analyses revealed that major magnetotactic taxonomic groups can be accurately determined only with coordinated scanning electron microscopy observations on fluorescently labeled single cells due to limited group coverage and specificity for existing group-specific MTB fluorescence in situ hybridization (FISH) probes. Our reported strategy is simple and efficient, offers great promise toward investigating the diversity and biomineralization of MTB, and may also be applied to other functional groups of microorganisms.IMPORTANCE Magnetotactic bacteria (MTB) are phylogenetically diverse and biomineralize morphologically diverse magnetic nanocrystals of magnetite or greigite in intracellular structures termed magnetosomes. However, many uncultured MTB strains have not been phylogenetically identified or structurally investigated at the single-cell level, which limits our comprehensive understanding of the diversity of MTB and their role in biomineralization. We developed a fluorescence-coupled electron microscopy method for the rapid phylogenetic and biomineralogical characterization of uncultured MTB at the single-cell level. Using this novel method, we successfully identified taxonomic groups of several uncultured MTB and one novel magnetotactic Gammaproteobacteria strain, SHHR-1, from natural environments. Our analyses further indicate that strain SHHR-1 forms elongated prismatic magnetites. Our findings provide a promising strategy for the rapid characterization of phylogenetic and biomineralogical properties of uncultured MTB at the single-cell level. Furthermore, due to its simplicity and generalized methodology, this strategy can also be useful in the study of the diversity and biomineralization properties of microbial taxa involved in other mineralization processes.

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Constant Flux of Spatial Niche Partitioning through High-Resolution Sampling of Magnetotactic Bacteria.

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