Accumulation and Dissolution of Magnetite Crystals in a Magnetically Responsive Ciliate

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.