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    Accumulation and Dissolution of Magnetite Crystals in a Magnetically Responsive Ciliate

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    Applied and Environmental ...
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    Authors
    Monteil, CL
    Menguy, N
    Prévéral, S
    Warren, A cc
    Pignol, D
    Lefèvre, CT
    Editors
    Kelly, RM
    Issue date
    2018-02-09
    Submitted date
    2018-03-20
    Subject Terms
    biomineralization
    grazing
    iron cycling
    magnetite
    magnetotactic bacteria
    protozoa
    
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    Show full item record
    Abstract
    Magnetotactic bacteria (MTB) represent a group of microorganisms that are widespread in aquatic habitats and thrive at the oxic-anoxic interfaces. They are able to scavenge high concentrations of iron thanks to the biomineralization of magnetic crystals in their unique organelle, the so-called magnetosome chain. Although their biodiversity has been intensively studied in recent years, their ecology and impact on iron cycling remain largely unexplored. Predation by protozoa was suggested as one of the ecological processes that could be involved in the release of iron back into the ecosystem. Magnetic protozoa have previously been observed in aquatic environments, but their diversity and the fate of particulate iron during grazing are poorly documented. In this study, we report the morphological and molecular characterization of a magnetically responsive MTB-grazing protozoan able to ingest high quantities of MTB. This protozoan is tentatively identified as Uronema marinum, a ciliate known to be a bacteria predator. Using light and electron microscopy, we investigate in detail the vacuoles in which lysis of phagocytized prokaryotes occurs. We carried out high-resolution observations of aligned magnetosome chains and ongoing dissolution of crystals. Particulate iron in the ciliate represented about 0.01% of its total volume. We show the ubiquity of this interaction in other types of environments and describe different grazing strategies. These data contribute to the mounting evidence that interaction between MTB-protozoan might play a significant role in iron turnover in microaerophilic habitats. IMPORTANCE Identifying participants of each biogeochemical cycle is a prerequisite to our understanding of ecosystems functioning. Magnetotactic bacteria (MTB) participate to iron cycling by concentrating large amounts of biomineralized iron minerals into their cells, which impacts their chemical environment at or below the oxic-anoxic transition zone in aquatic habitats. It was shown that some protozoa inhabiting this niche could become magnetic with the ingestion of magnetic crystals biomineralized by grazed MTB. In this study, we show that magnetic MTB-grazers are commonly observed in marine and freshwater sediments and can sometimes accumulate very large amounts of particulate iron. Using magnetic particles from MTB as tracers after their ingestion by the protozoa, different phagocytosis strategies are described. This study paves the way for potential scientific or medical applications using MTB-grazers as magnetosome-hyperaccumulators.
    Citation
    Accumulation and dissolution of magnetite crystals in a magnetically responsive ciliate Caroline L. Monteil, Nicolas Menguy, Sandra Prévéral, Alan Warren, David Pignol, Christopher T. Lefèvre Applied and Environmental Microbiology Feb 2018, AEM.02865-17; DOI: 10.1128/AEM.02865-17
    Publisher
    American Society of Microbiology
    Journal
    Applied and Environmental Microbiology
    URI
    http://hdl.handle.net/10141/622547
    DOI
    10.1128/AEM.02865-17
    Type
    Journal Article
    Item Description
    Copyright © 2018 American Society for Microbiology. This document is the author’s final accepted version of the journal article. You are advised to consult the published version if you wish to cite from it.
    NHM Repository
    ISSN
    0099-2240
    EISSN
    1098-5336
    ae974a485f413a2113503eed53cd6c53
    10.1128/AEM.02865-17
    Scopus Count
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    Life sciences

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