Light irradiation helps magnetotactic bacteria eliminate intracellular reactive oxygen species

Li, Kefeng; Wang, Pingping; Chen, Chuanfang; Chen, Changyou; Li, Lulu; Song, Tao

doi:10.1111/1462-2920.13864

Cited by 16 publications

(29 citation statements)

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“…On early Earth, the lack of a protective ozone layer resulted in higher harmful ultraviolet radiation than the present-day Earth, which would have been a major challenge for life in surface and shallow-water conditions [ 82 ]. The intrinsic enzyme-like properties of magnetosomal iron nanoparticles [ 17 , 18 ] and the stability of Fe 3 O 4 nanozyme under a wide range of temperatures (4 to 90 °C) and pH (1 to 12) [ 83 ] might have helped life to cope with environmental stresses on early Earth (e.g., detoxification of ultraviolet radiation (UVR) and free-iron-generated ROS [ 12 ]). In addition, magnetotaxis behaviour may have also protected early MTB from lethal UVR by allowing efficient geomagnetic-field-directed swimming from near surface and shallow-water microenvironments to deeper water or sediment [ 84 ].…”

Section: Resultsmentioning

confidence: 99%

“…Magnetic particles within MTB magnetosomes are typically organized into (a) chain-like structure(s) within the cell in order to optimize the cellular magnetic dipole moment. Functions of magnetosomes include magnetoreception [ 15 , 16 ] and ROS detoxification [ 17 , 18 ], both of which have been experimentally proven. Additional proposed functions, such as iron storage and sequestration, acting as an electrochemical battery or a gravity sensor, need further testing.…”

Section: Introductionmentioning

confidence: 99%

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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: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Expanding magnetic organelle biogenesis in the domain Bacteria

et al. 2020

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“…On early Earth the lack of a protective ozone layer resulted in higher harmful ultraviolet radiation than the present-day Earth, which would have been one of major challenges for life in the surface and shallow-water conditions 77 . The intrinsic enzyme-like properties of magnetosome iron nanoparticles 78,79 and their potentially enhanced enzyme-like stability under a wide range of temperatures and pH 80 might have helped life to cope with environmental stresses on early Earth (e.g., detoxification of ultraviolet radiation and free-iron-generated ROS 12 ). No MGC has yet been found in the Archaea , which suggests that magnetosomal biogenesis evolved after the divergence of Bacteria and Archaea .…”

Section: Resultsmentioning

confidence: 99%

“…Magnetic particles within MTB magnetosomes are typically organized into (a) chain-like structure(s) within the cell in order to optimize the cellular magnetic dipole moment. Functions of magnetosomes include magnetoreception 103,104 and ROS detoxification 78,79 , both of which have been experimentally proven. Additional proposed functions, such as iron storage and sequestration, acting as an electrochemical battery or a gravity sensor, need further testing.…”

Section: Introductionmentioning

confidence: 99%

Expanding magnetic organelle biogenesis in the domainBacteria

Lin

Zhang

Paterson

et al. 2020

Preprint

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21The discovery of membrane-enclosed, metabolically functional organelles in 22 Bacteria and Archaea has transformed our understanding of the subcellular 23 complexity of prokaryotic cells. However, whether prokaryotic organelles 24 emerged early or late in evolutionary history remains unclear and limits 25 understanding of the nature and cellular complexity of early life. 26 Biomineralization of magnetic nanoparticles within magnetosomes by 27 magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. 28 Here, we reconstruct 168 metagenome-assembled MTB genomes from various 29 aquatic environments and waterlogged soils. These genomes represent nearly a 3-30 fold increase over the number currently available, and more than double the 31 known MTB species. Phylogenomic analysis reveals that these newly described 32 genomes belong to 13 Bacterial phyla, six of which were previously not known to 33 include MTB. These findings indicate a much wider taxonomic distribution of 34 magnetosome organelle biogenesis across the domain Bacteria than previously 35 thought. Comparative genome analysis reveals a vast diversity of magnetosome 36 gene clusters involved in magnetosomal biogenesis in terms of gene content and 37 synteny residing in distinct taxonomic lineages. These gene clusters therefore 38 represent a promising, diverse genetic resource for biosynthesizing novel magnetic 39 nanoparticles. Finally, our phylogenetic analyses of the core magnetosome 40 proteins in this largest available and taxonomically diverse dataset support an 41 unexpectedly early evolutionary origin of magnetosome biomineralization, likely 42 ancestral to the origin of the domain Bacteria. These findings emphasize the 43 potential biological significance of prokaryotic organelles on the early Earth and 44 have important implications for our understanding of the evolutionary history of 45 cellular complexity.46 47It was accepted widely that intracellular, membrane-bounded, metabolically functional 48 organelles are present exclusively in eukaryotic cells and that they are absent from 49 Bacteria and Archaea. This long-held view was revised after numerous recent 50 discoveries of a diverse group of highly organized, membrane-enclosed organelles in 51 the domains Bacteria and Archaea associated with specific cellular functions 1-3 . 52However, the origin and evolution of prokaryotic organelles remain largely elusive. It 53 is still unclear whether organelle biogenesis emerged early or late during the evolution 54 of Bacteria and Archaea, posing problems for elucidating the evolutionary history of 55 cellular complexity. 56 Magnetosomes within magnetotactic bacteria (MTB) are a striking example of 57 prokaryotic organelles 4 . Magnetosomes consist of a lipid bilayer-bounded membrane 58 in which nanosized, ferrimagnetic magnetite (Fe3O4) and/or greigite (Fe3S4) crystals 59 are biomineralized and usually arranged in chain-like structure(s) that maximize the 60 magnetic dipole moment 5,6 (Figure 1). The most accepted maj...

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“…Illumination also influences the growth and magnetosome synthesis of cultured MTB [15–17]. Recent research found that Magnetospirillum magneticum AMB-1, a well-studied MTB strain, was able to not only swim towards visible light [15] but also increase magnetosome synthesis and upregulate stress-related genes [16]. Ultraviolet illumination can delay AMB-1 cell growth and induce both cellular and DNA damage [17].…”

Section: Introductionmentioning

confidence: 99%

Genomic evidence of the illumination response mechanism and evolutionary history of magnetotactic bacteria within the Rhodospirillaceae family

et al. 2019

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Background Magnetotactic bacteria (MTB) are ubiquitous in natural aquatic environments. MTB can produce intracellular magnetic particles, navigate along geomagnetic field, and respond to light. However, the potential mechanism by which MTB respond to illumination and their evolutionary relationship with photosynthetic bacteria remain elusive. Results We utilized genomes of the well-sequenced genus Magnetospirillum , including the newly sequenced MTB strain Magnetospirillum sp. XM-1 to perform a comprehensive genomic comparison with phototrophic bacteria within the family Rhodospirillaceae regarding the illumination response mechanism. First, photoreceptor genes were identified in the genomes of both MTB and phototrophic bacteria in the Rhodospirillaceae family, but no photosynthesis genes were found in the MTB genomes. Most of the photoreceptor genes in the MTB genomes from this family encode phytochrome-domain photoreceptors that likely induce red/far-red light phototaxis. Second, illumination also causes damage within the cell, and in Rhodospirillaceae, both MTB and phototrophic bacteria possess complex but similar sets of response and repair genes, such as oxidative stress response, iron homeostasis and DNA repair system genes. Lastly, phylogenomic analysis showed that MTB cluster closely with phototrophic bacteria in this family. One photoheterotrophic genus, Phaeospirillum , clustered within and displays high genomic similarity with Magnetospirillum . Moreover, the phylogenetic tree topologies of magnetosome synthesis genes in MTB and photosynthesis genes in phototrophic bacteria from the Rhodospirillaceae family were reasonably congruent with the phylogenomic tree, suggesting that these two traits were most likely vertically transferred during the evolution of their lineages. Conclusion Our new genomic data indicate that MTB and phototrophic bacteria within the family Rhodospirillaceae possess diversified photoreceptors that may be responsible for phototaxis. Their genomes also contain comprehensive stress response genes to mediate the negative effects caused by illumination. Based on phylogenetic studies, most of MTB and phototrophic bacteria in the Rhodospirillaceae family evolved vertically with magnetosome synthesis and photosynthesis genes. The ancestor of Rhodospirillaceae was likely a magnetotactic phototrophic bacteria, however, gain or loss of magnetotaxis and phototrophic abilities might have occurred during the evolution of ancestral Rhodospirillaceae lineages. Electronic supplementary material The online version of this article (10.1186/s12864-019-5751-9) contains supplementary material, which is available to authorized users.

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Light irradiation helps magnetotactic bacteria eliminate intracellular reactive oxygen species

Cited by 16 publications

References 41 publications

Expanding magnetic organelle biogenesis in the domain Bacteria

Expanding magnetic organelle biogenesis in the domain Bacteria

Expanding magnetic organelle biogenesis in the domainBacteria

Genomic evidence of the illumination response mechanism and evolutionary history of magnetotactic bacteria within the Rhodospirillaceae family

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