Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Amor, Matthieu; Tharaud, Mickaël; Gélabert, Alexandre; Komeili, Arash

doi:10.1111/1462-2920.14708

Cited by 48 publications

(52 citation statements)

References 41 publications

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“…However, few studies have reported MTB in waterlogged soils [ 22 , 23 ]. Magnetosomal biogenesis by MTB is recognized as a key component of the global iron cycle [ 24 , 25 ], and MTB cells are potentially important in the biogeochemical cycling of carbon, phosphorus, nitrogen, and sulphur [ 9 , 26 – 28 ]. Historically, magnetosomal biomineralization has been viewed as a specialized type of metabolism restricted to two Bacterial phyla: the Proteobacteria ( Alphaproteobacteria , Deltaproteobacteria , and Gammaproteobacteria classes) and the Nitrospirae [ 29 ].…”

Section: Introductionmentioning

confidence: 99%

Expanding magnetic organelle biogenesis in the domain Bacteria

et al. 2020

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Background The discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells. Biomineralization of magnetic nanoparticles within magnetosomes by magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. Magnetosomes, as nano-sized magnetic sensors in MTB, facilitate cell navigation along the local geomagnetic field, a behaviour referred to as magnetotaxis or microbial magnetoreception. Recent discovery of novel MTB outside the traditionally recognized taxonomic lineages suggests that MTB diversity across the domain Bacteria are considerably underestimated, which limits understanding of the taxonomic distribution and evolutionary origin of magnetosome organelle biogenesis. Results Here, we perform the most comprehensive metagenomic analysis available of MTB communities and reconstruct metagenome-assembled MTB genomes from diverse ecosystems. Discovery of MTB in acidic peatland soils suggests widespread MTB occurrence in waterlogged soils in addition to subaqueous sediments and water bodies. A total of 168 MTB draft genomes have been reconstructed, which represent nearly a 3-fold increase over the number currently available and more than double the known MTB species at the genome level. Phylogenomic analysis reveals that these genomes belong to 13 Bacterial phyla, six of which were previously not known to include MTB. These findings indicate a much wider taxonomic distribution of magnetosome organelle biogenesis across the domain Bacteria than previously thought. Comparative genome analysis reveals a vast diversity of magnetosome gene clusters involved in magnetosomal biogenesis in terms of gene content and synteny residing in distinct taxonomic lineages. Phylogenetic analyses of core magnetosome proteins in this largest available and taxonomically diverse dataset support an unexpectedly early evolutionary origin of magnetosome biomineralization, likely ancestral to the origin of the domain Bacteria. Conclusions These findings expand the taxonomic and phylogenetic diversity of MTB across the domain Bacteria and shed new light on the origin and evolution of microbial magnetoreception. Potential biogenesis of the magnetosome organelle in the close descendants of the last bacterial common ancestor has important implications for our understanding of the evolutionary history of bacterial cellular complexity and emphasizes the biological significance of the magnetosome organelle.

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Section: Introductionmentioning

confidence: 99%

Expanding magnetic organelle biogenesis in the domain Bacteria

et al. 2020

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“…In the process of biomineralization of magnetite or greigite, MTB take up large amounts of dissolved iron from the surrounding environment and sequester it in magnetosomes as iron crystals. As such, the role that MTB play in iron cycling in both freshwater bodies and the ocean is potentially quite large [5,8]. Conservative estimates from Amor and colleagues indicate that estuarine and oceanic MTB may take up anywhere from approximately 1% to 50% of dissolved iron inputs (approximately 9 × 10 8 kg per year) in their environments [8].…”

Section: Introductionmentioning

confidence: 99%

“…As such, the role that MTB play in iron cycling in both freshwater bodies and the ocean is potentially quite large [5,8]. Conservative estimates from Amor and colleagues indicate that estuarine and oceanic MTB may take up anywhere from approximately 1% to 50% of dissolved iron inputs (approximately 9 × 10 8 kg per year) in their environments [8]. Having a greater understanding of the iron regulation strategies encoded within the genomes of MTB, as well as how iron is taken up and distributed to magnetosomes, is important for a more accurate picture of the role of MTB in their aquatic environments.…”

Section: Introductionmentioning

confidence: 99%

Magnetic genes: Studying the genetics of biomineralization in magnetotactic bacteria

McCausland

Komeili

2020

PLoS Genet

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Many species of bacteria can manufacture materials on a finer scale than those that are synthetically made. These products are often produced within intracellular compartments that bear many hallmarks of eukaryotic organelles. One unique and elegant group of organisms is at the forefront of studies into the mechanisms of organelle formation and biomineralization. Magnetotactic bacteria (MTB) produce organelles called magnetosomes that contain nanocrystals of magnetic material, and understanding the molecular mechanisms behind magnetosome formation and biomineralization is a rich area of study. In this Review, we focus on the genetics behind the formation of magnetosomes and biomineralization. We cover the history of genetic discoveries in MTB and key insights that have been found in recent years and provide a perspective on the future of genetic studies in MTB.

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“…Lastly, spICP‐MS can provide the elemental compositions of hundreds to thousands of suspended nanoparticle aggregates within minutes (Lee et al ., 2014; Bevers et al, 2020). A derivation of this technique has already been used to probe the variation in Fe content of magnetotactic bacteria at the single cell levels using single‐cell ICP‐MS (Amor et al ., 2020). All of these techniques will be capable of probing microbe‐nanoparticle interactions at an unprecedented scale.…”

Section: Future Directionsmentioning

confidence: 99%

Benefits at the nanoscale: a review of nanoparticle‐enabled processes favouring microbial growth and functionality

Mansor

2020

Environmental Microbiology

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Nanoparticles are ubiquitous and co-occur with microbial life in every environment on Earth. Interactions between microbes and nanoparticles impact the biogeochemical cycles via accelerating various reaction rates and enabling biological processes at the smallest scales. Distinct from microbe-mineral interactions at large, microbe-nanoparticle interactions may involve higher levels of active recognition and utilization of the reactive, changeable, and thereby 'moldable' nano-sized inorganic phases by microbes, which has been given minimal attention in previous reviews. Here we have compiled the various cases of microbe-nanoparticle interactions with clear and potential benefits to the microbial cells and communities. Specifically, we discussed (i) the high bioavailabilities of nanoparticles due to increased specific surface areas and size-dependent solubility, with a focus on environmentally-relevant iron(III) (oxyhydr)oxides and pyrite, (ii) microbial utilization of nanoparticles as 'nano-tools' for electron transfer, chemotaxis, and storage units, and (iii) speculated benefits of precipitating 'moldable' nanoparticles in extracellular biomineralization. We further discussed emergent questions concerning cellular level responses to nanoparticle-associated cues, and the factors that affect nanoparticles' bioavailabilities beyond sizedependent effects. We end the review by proposing a framework towards more quantitative approaches and by highlighting promising techniques to guide future research in this exciting field.

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Single‐cell determination of iron content in magnetotactic bacteria: implications for the iron biogeochemical cycle

Cited by 48 publications

References 41 publications

Expanding magnetic organelle biogenesis in the domain Bacteria

Expanding magnetic organelle biogenesis in the domain Bacteria

Magnetic genes: Studying the genetics of biomineralization in magnetotactic bacteria

Benefits at the nanoscale: a review of nanoparticle‐enabled processes favouring microbial growth and functionality

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