Genome-Based Metabolic Reconstruction of a Novel Uncultivated Freshwater Magnetotactic coccus “Ca. Magnetaquicoccus inordinatus” UR-1, and Proposal of a Candidate Family “Ca. Magnetaquicoccaceae”

Koziaeva, Veronika; Dziuba, Marina; Leão, Pedro; Uzun, Maria; Krutkina, Maria S.; Grouzdev, Denis S.

doi:10.3389/fmicb.2019.02290

Cited by 34 publications

(25 citation statements)

References 111 publications

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“…In the past decade, significant progress has been made in identifying MTB from natural environments using culture‐independent analysis methods at the single‐cell level (Kolinko et al, 2012; Li et al, 2017). For instance, by coupling fluorescence in situ hybridization (FISH) analysis with transmission or scanning electron microscope (TEM or SEM) observation, a so‐called coupled FISH‐SEM or FISH‐TEM approach, MTB cells from natural environments can be identified phylogenetically and structurally at the single‐cell level (Koziaeva et al, 2019; Li et al, 2017, 2019; Qian et al, 2019, 2020; Zhang et al, 2017). On the other hand, rapid development of metagenomics and single‐cell genomics has enabled identification of more magnetosome gene clusters (MGCs) responsible for magnetosome biomineralization in uncultured MTB (Jogler et al, 2011; Kolinko et al, 2014, 2016; Lin et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Menguy

Roberts

et al. 2020

JGR Biogeosciences

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Magnetite produced by magnetotactic bacteria (MTB) provides stable paleomagnetic signals because it occurs as natural single‐domain magnetic nanocrystals. MTB can also provide useful paleoenvironmental information because their crystal morphologies are associated with particular bacterial groups and the environments in which they live. However, identification of the fossil remains of MTB (i.e., magnetofossils) from ancient sediments or rocks is challenging because of their generally small sizes and because the growth, morphology, and chain assembly of magnetite within MTB are not well understood. Nanoscale characterization is, therefore, needed to understand magnetite biomineralization and to develop magnetofossils as biogeochemical proxies for paleoenvironmental reconstructions. Using advanced transmission electron microscopy, we investigated magnetite growth and chain arrangements within magnetotactic Deltaproteobacteria strain WYHR‐1, which reveals how the magnetite grows to form elongated, bullet‐shaped nanocrystals. Three crystal growth stages are recognized: (i) initial isotropic growth to produce nearly round ~20 nm particles, (ii) subsequent anisotropic growth along the [001] crystallographic direction to ~75 nm lengths and ~30–40 nm widths, and (iii) unidirectional growth along the [001] direction to ~180 nm lengths, with some growing to ~280 nm. Crystal growth and habit differ from that of magnetite produced by other known MTB strains, which indicates species‐specific biomineralization. These findings suggest that magnetite biomineralization might be much more diverse among MTB than previously thought. When characterized adequately at species level, magnetofossil crystallography, and apomorphic features are, therefore, likely to become useful proxies for ancient MTB taxonomic groups or species and for interpreting the environments in which they lived.

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Section: Introductionmentioning

confidence: 99%

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Menguy

Roberts

et al. 2020

JGR Biogeosciences

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“…The compared trees also indicated vertical inheritance in the Alpha-and Ca. Etaproteobacteria groups, although the occurrence of horizontal transfer events was previously established in these groups 27,31 . These types of transfers have been confirmed to have occurred recently, which is why they cannot be detected through the tree topology analysis.…”

Section: Reconstruction Of the Evolutionary Pathways For Mgcs The Idmentioning

confidence: 84%

“…Etaproteobacteria class. Genomes from this class previously were found in both saline and freshwater habitats 15,31,53 . The obtained MAG clustered with genomes isolated from freshwater environments.…”

Section: The Search For Magnetosome Biomineralization Genes In Open Dmentioning

confidence: 88%

Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases

et al. 2020

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Magnetotactic bacteria (MtB) are prokaryotes that possess genes for the synthesis of membranebounded crystals of magnetite or greigite, called magnetosomes. Despite over half a century of studying MTB, only about 60 genomes have been sequenced. Most belong to Proteobacteria, with a minority affiliated with the Nitrospirae, Omnitrophica, Planctomycetes, and Latescibacteria. Due to the scanty information available regarding MTB phylogenetic diversity, little is known about their ecology, evolution and about the magnetosome biomineralization process. This study presents a large-scale search of magnetosome biomineralization genes and reveals 38 new MTB genomes. Several of these genomes were detected in the phyla Elusimicrobia, Candidatus Hydrogenedentes, and Nitrospinae, where magnetotactic representatives have not previously been reported. Analysis of the obtained putative magnetosome biomineralization genes revealed a monophyletic origin capable of putative greigite magnetosome synthesis. The ecological distributions of the reconstructed MTB genomes were also analyzed and several patterns were identified. These data suggest that open databases are an excellent source for obtaining new information of interest.

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“…In recent years, the known extent of MTB diversity has undergone a significant expansion due to methodological advances, such as the successful cultivation of novel MTB strains e.g., 29–32 , 16S rRNA gene-based characterization e.g., 33–35 , genome mining of public repositories including GenBank and IMG/ER 17,36 , and cultivation-independent surveys of magnetosome gene clusters (MGCs, which are physically clustered groups of genes that are together responsible for magnetosomal biogenesis) 37,38 . MTB have now been further identified in other Bacterial taxa, including the Betaproteobacteria , Zetaproteobacteria , “ Candidatus Etaproteobacteria”, and “ Candidatus Lambdaproteobacteria” classes of the Proteobacteria phylum, the candidate phylum Omnitrophica (previously known as the candidate division OP3), the candidate phylum Latescibacteria (previously known as the candidate division WS3), and the phylum Planctomycetes , according to the NCBI taxonomy.…”

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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Genome-Based Metabolic Reconstruction of a Novel Uncultivated Freshwater Magnetotactic coccus “Ca. Magnetaquicoccus inordinatus” UR-1, and Proposal of a Candidate Family “Ca. Magnetaquicoccaceae”

Cited by 34 publications

References 111 publications

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases

Expanding magnetic organelle biogenesis in the domainBacteria

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