Origin of microbial biomineralization and magnetotaxis during the Archean

Lin, Wei; Paterson, Greig A.; Zhu, Qiyun; Wang, Yinzhao; Kopylova, Evguenia; Liu, Ying; Knight, Rob; Bazylinski, Dennis A.; Zhu, Rixiang; Kirschvink, Joseph L.; Pan, Yongxin

doi:10.1073/pnas.1614654114

Cited by 104 publications

(119 citation statements)

References 70 publications

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“…Recently, Lin and colleagues () proposed that magnetotaxis in MTB developed during the Archean, suggesting that magnetoreception and the Earth's magnetic field evolved together over time. Understanding the origin and evolution of magnetoreception is clearly important in understanding mechanisms of magnetoreception currently utilized by organisms and possibly to predict future developments in this area, especially in view of the recent unexpected changes in Earth's magnetic field (Witze, ).…”

Section: Introductionmentioning

confidence: 97%

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

Leão

Nagard

Yuan

et al. 2019

Environmental Microbiology

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Summary The most well‐recognized magnetoreception behaviour is that of the magnetotactic bacteria (MTB), which synthesize membrane‐bounded magnetic nanocrystals called magnetosomes via a biologically controlled process. The magnetic minerals identified in prokaryotic magnetosomes are magnetite (Fe3O4) and greigite (Fe3S4). Magnetosome crystals, regardless of composition, have consistent, species‐specific morphologies and single‐domain size range. Because of these features, magnetosome magnetite crystals possess specific properties in comparison to abiotic, chemically synthesized magnetite. Despite numerous discoveries regarding MTB phylogeny over the last decades, this diversity is still considered underestimated. Characterization of magnetotactic microorganisms is important as it might provide insights into the origin and establishment of magnetoreception in general, including eukaryotes. Here, we describe the magnetotactic behaviour and characterize the magnetosomes from a flagellated protist using culture‐independent methods. Results strongly suggest that, unlike previously described magnetotactic protists, this flagellate is capable of biomineralizing its own anisotropic magnetite magnetosomes, which are aligned in complex aggregations of multiple chains within the cell. This organism has a similar response to magnetic field inversions as MTB. Therefore, this eukaryotic species might represent an early origin of magnetoreception based on magnetite biomineralization. It should add to the definition of parameters and criteria to classify biogenic magnetite in the fossil record.

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Section: Introductionmentioning

confidence: 97%

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

Leão

Nagard

Yuan

et al. 2019

Environmental Microbiology

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“…In sediments or water column, MTB are markers of oxic/anoxic transition zones (OATZ) where the concentration of dissolved iron is at its maximum (Kopp and Kirschvink, 2008;Lefèvre and Bazylinski, 2013). MTB have been proposed to represent some of the most ancient organisms capable of biomineralization, with an origin dating back to at least 3 Ga (Lin et al, 2017). Although MTB are ubiquitous on Earth, their impact on the past and modern biogeochemical cycling of metallic elements is still poorly constrained.…”

Section: Introductionmentioning

confidence: 99%

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

Amor

Tharaud

Gélabert

et al. 2019

Environmental Microbiology

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Summary Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that mineralize dissolved iron into intracellular magnetic crystals. After cell death, these crystals are trapped into sediments that remove iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits nitrogen fixation and primary productivity. A thorough assessment of their impact has been hampered by a lack of methodology to measure the amount of, and variability in, their intracellular iron content. We quantified the iron mass contained in single MTB cells of Magnetospirillum magneticum strain AMB‐1 using a time‐resolved inductively coupled plasma‐mass spectrometry methodology. Bacterial iron content depends on the external iron concentration, and reaches a maximum value of ~10−6 ng of iron per cell. From these results, we calculated the flux of dissolved iron incorporation into environmental MTB populations and conclude that MTB may mineralize a significant fraction of dissolved iron into crystals.

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“…Being one of the deep-branching MTB group, Nitrospirae MTB plays an important role when analysing the origin and evolution of magnetosome biomineralization and magnetotaxis. Lin et al suggested that the magnetosome biomineralization and magnetotaxis was present before the separation of the Nitrospirae and Proteobacteria phyla, which was between~3.38 and 3.21 Ga (Lin et al, 2017b). However, it remains unclear whether the acquisition of magnetosome island (MAI), that encodes essential proteins for magnetosome biosynthesis in the genome, occurred before or after the divergence between freshwater and marine Nitrospirae MTB.…”

Section: Phylogenetic Analysismentioning

confidence: 99%

Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum

Qian

Liu

Menguy

et al. 2019

Environ Microbiol Rep

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Summary Magnetotactic bacteria (MTB) are a group of Gram‐negative bacteria characterized by synthesizing magnetosomes and swimming along geomagnetic field lines. Phylogenetically, they belong to different taxonomic lineages including Proteobacteria, Nitrospirae, Omnitrophica, Latescibacteria and Planctomycetes phyla on the phylogenetic tree. To date, six Nitrospirae MTB phylotypes have been identified from freshwater or low‐salinity environments and described in the literature. Here, we report the identification of two Nitrospirae MTB phylotypes collected, for the first time, from the marine environment. Both have a spherical morphology with a cell size of ~ 5 μM and similar motility but are different colours (black‐brown and ivory‐white) under the optic microscope. They synthesized bullet‐shaped iron‐oxide magnetosomes that were arranged in multiple bundles of chains. Moreover, the cytoplasm of the black‐brown Nitrospirae MTB contained sulphur inclusions that conferred on cells a rough, granular appearance. Phylogenetic analysis based on their 16S rRNA gene sequences revealed that they are two novel species and cluster with the previously reported MTB affiliated with the phylum Nitrospirae, thus extending the distribution of Nitrospirae MTB from freshwater to the marine environment.

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Origin of microbial biomineralization and magnetotaxis during the Archean

Cited by 104 publications

References 70 publications

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

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

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

Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum

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