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 oxic-anoxic interfaces. They are able to scavenge high concentrations of iron thanks to the biomineralization of magnetic crystals in their unique organelles, the so-called magnetosome chains. Although their biodiversity has been intensively studied, 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 were previously 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 characterizations of a magnetically responsive MTB-grazing protozoan able to ingest high quantities of MTB. This protozoan is tentatively identified as , a ciliate known to be a predator of bacteria. Using light and electron microscopy, we investigated in detail the vacuoles in which the 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 approximately 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 the interactions between MTB and protozoa might play a significant role in iron turnover in microaerophilic habitats. Identifying participants of each biogeochemical cycle is a prerequisite to our understanding of ecosystem functioning. Magnetotactic bacteria (MTB) participate in iron cycling by concentrating large amounts of biomineralized iron minerals in 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 by 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. We describe here different phagocytosis strategies, determined using magnetic particles from MTB as tracers after their ingestion by the protozoa. This study paves the way for potential scientific or medical applications using MTB grazers as magnetosome hyperaccumulators.

Magnetoreception in Microorganisms

“…In this study, it was not possible to state if this behaviour occurs in environmental conditions and if magnetoreception could arise from the interaction. Recently, this behaviour was investigated in natural populations of protists and MTB, and it was shown that ciliates affiliated to the genus Uronema (Stramenopiles-Alveolates-Rhizaria, SAR group) were able to ingest hundreds of MTB into acidic vacuoles to progressively become sensitive to the variations of the magnetic fields in the same way than MTB (Figure 2A and B) [11]. The magnetic response in MTB-grazers is certainly not encoded in the eukaryote genome, but this behaviour seems to facilitate movement of grazers towards the prey biomass.…”

“…However, the directed grazing towards these preys specifically and the magnetic response suggest that this interaction is widespread among marine and freshwater heterotrophic flagellates and ciliates ( Figure 2). MTB-grazers seem to have evolved different strategies for the internalization of MTB and their magnetosome chains: (i) sequestration in food vacuoles (Figure 2A and B), (ii) accumulation in a specific location in the cell ( Figure 2C and D), and (iii) an apparently random storage in the cell (Figure 2E) [11,48,50]. These magnetically responsive protists also appear to have evolved different strategies to deal with iron toxicity with (i) the egestion of magnetic inclusions where magnetosomes accumulated [48] and (ii) the progressive dissolution of magnetosomes until the colloidal iron would be expelled from the protistan cell via the cytoproct [11,50,51].…”

“…This behaviour, called magnetotaxis, was until recently, observed in magnetotactic bacteria only. However, recent discoveries revealed that some unicellular eukaryotes in different phylogenetic groups are magnetotactic or at least become transiently magnetoreceptive by different mechanisms and interactions [11,12]. Here, we propose to review the diversity and different strategies microbes have developed to obtain their magnetic sense.…”

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes

“…In one type, they appeared to be in vacuoles and were extruded from the cell without apparent harm, although no longer displaying magnetotaxis. Further analysis of those magnetic protists revealed that magnetosome‐like structures found inside these organisms were identical to those found in MTB present in the same environment (Bazylinski et al ., ), suggesting that the magnetosome‐like structures were not biomineralized by the protists but accumulated inside the cells through ingestion of MTB (Monteil et al ., ). Torres de Araujo and colleagues () described a single‐celled eukaryotic alga presenting a magnetotactic behaviour more typical of MTB.…”

A species of magnetotactic deltaproteobacterium was detected at the highest abundance during an algal bloom

“…MTB are prey for protozoa, and this is one of the likely pathways for return of iron to the environment (Bazylinski, et al 2000, Lin, et al 2014a, Monteil, et al 2018. In Lvdao Lake the digestion of magnetosomes in the food vacuoles of protozoa during grazing on MTB could generate bioavailable iron for cyanobacteria.…”