Literature DB >> 34756060

A Novel Magnetotactic Alphaproteobacterium Producing Intracellular Magnetite and Calcium-Bearing Minerals.

Peiyu Liu1,2,3, Yan Liu1,2,3, Xinyi Ren4,5, Zhifei Zhang4,5, Xiang Zhao6, Andrew P Roberts6, Yongxin Pan1,3, Jinhua Li1,2,3.   

Abstract

Magnetotactic bacteria (MTB) are prokaryotes that form intracellular magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals with tailored sizes, often in chain configurations. Such magnetic particles are each surrounded by a lipid bilayer membrane, called a magnetosome, and provide a model system for studying the formation and function of specialized internal structures in prokaryotes. Using fluorescence-coupled scanning electron microscopy, we identified a novel magnetotactic spirillum, XQGS-1, from freshwater Xingqinggong Lake, Xi'an City, Shaanxi Province, China. Phylogenetic analyses based on 16S rRNA gene sequences indicate that strain XQGS-1 represents a novel genus of the Alphaproteobacteria class in the Proteobacteria phylum. Transmission electron microscopy analyses reveal that strain XQGS-1 forms on average 17 ± 3 magnetite magnetosome particles with an ideal truncated octahedral morphology, with an average length and width of 88.3 ± 11.7 nm and 83.3 ± 11.0 nm, respectively. They are tightly organized into a single chain along the cell long axis close to the concave side of the cell. Intrachain magnetic interactions likely result in these large equidimensional magnetite crystals behaving as magnetically stable single-domain particles that enable bacterial magnetotaxis. Combined structural and chemical analyses demonstrate that XQGS-1 cells also biomineralize intracellular amorphous calcium phosphate (2 to 3 granules per cell; 90.5- ± 19.3-nm average size) and weakly crystalline calcium carbonate (2 to 3 granules per cell; 100.4- ± 21.4-nm average size) in addition to magnetite. Our results expand the taxonomic diversity of MTB and provide evidence for intracellular calcium phosphate biomineralization in MTB. IMPORTANCE Biomineralization is a widespread process in eukaryotes that form shells, teeth, or bones. It also occurs commonly in prokaryotes, resulting in more than 60 known minerals formed by different bacteria under wide-ranging conditions. Among them, magnetotactic bacteria (MTB) are remarkable because they might represent the earliest organisms that biomineralize intracellular magnetic iron minerals (i.e., magnetite [Fe3O4] or greigite [Fe3S4]). Here, we report a novel magnetotactic spirillum (XQGS-1) that is phylogenetically affiliated with the Alphaproteobacteria class. In addition to magnetite crystals, XQGS-1 cells form intracellular submicrometer calcium carbonate and calcium phosphate granules. This finding supports the view that MTB are also an important microbial group for intracellular calcium carbonate and calcium phosphate biomineralization.

Entities:  

Keywords:  biomineralization; calcium carbonate; calcium phosphate; magnetosome; magnetotactic bacteria

Mesh:

Substances:

Year:  2021        PMID: 34756060      PMCID: PMC8579999          DOI: 10.1128/AEM.01556-21

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  61 in total

1.  Habits of magnetosome crystals in coccoid magnetotactic bacteria.

Authors:  Ulysses Lins; Martha R McCartney; Marcos Farina; Richard B Frankel; Peter R Buseck
Journal:  Appl Environ Microbiol       Date:  2005-08       Impact factor: 4.792

2.  Magnetic microstructure of magnetotactic bacteria by electron holography

Authors: 
Journal:  Science       Date:  1998-12-04       Impact factor: 47.728

3.  Crystal growth of bullet-shaped magnetite in magnetotactic bacteria of the Nitrospirae phylum.

Authors:  Jinhua Li; Nicolas Menguy; Christophe Gatel; Victor Boureau; Etienne Snoeck; Gilles Patriarche; Eric Leroy; Yongxin Pan
Journal:  J R Soc Interface       Date:  2015-02-06       Impact factor: 4.118

4.  Measuring spectroscopy and magnetism of extracted and intracellular magnetosomes using soft X-ray ptychography.

Authors:  Xiaohui Zhu; Adam P Hitchcock; Dennis A Bazylinski; Peter Denes; John Joseph; Ulysses Lins; Stefano Marchesini; Hung-Wei Shiu; Tolek Tyliszczak; David A Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  2016-12-07       Impact factor: 11.205

5.  Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities.

Authors:  David W Waite; Maria Chuvochina; Claus Pelikan; Donovan H Parks; Pelin Yilmaz; Michael Wagner; Alexander Loy; Takeshi Naganuma; Ryosuke Nakai; William B Whitman; Martin W Hahn; Jan Kuever; Philip Hugenholtz
Journal:  Int J Syst Evol Microbiol       Date:  2020-11-05       Impact factor: 2.747

6.  The gammaproteobacterium Achromatium forms intracellular amorphous calcium carbonate and not (crystalline) calcite.

Authors:  Karim Benzerara; Romain Bolzoni; Caroline Monteil; Olivier Beyssac; Olivier Forni; Béatrice Alonso; Maria P Asta; Christopher Lefevre
Journal:  Geobiology       Date:  2020-12-21       Impact factor: 4.407

Review 7.  Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences.

Authors:  Pablo Yarza; Pelin Yilmaz; Elmar Pruesse; Frank Oliver Glöckner; Wolfgang Ludwig; Karl-Heinz Schleifer; William B Whitman; Jean Euzéby; Rudolf Amann; Ramon Rosselló-Móra
Journal:  Nat Rev Microbiol       Date:  2014-09       Impact factor: 60.633

8.  Genomic study of a novel magnetotactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis.

Authors:  Caroline L Monteil; Guy Perrière; Nicolas Menguy; Nicolas Ginet; Béatrice Alonso; Nicolas Waisbord; Stéphane Cruveiller; David Pignol; Christopher T Lefèvre
Journal:  Environ Microbiol       Date:  2018-10-16       Impact factor: 5.491

9.  Filamentous sulfur bacteria preserved in modern and ancient phosphatic sediments: implications for the role of oxygen and bacteria in phosphogenesis.

Authors:  J V Bailey; F A Corsetti; S E Greene; C H Crosby; P Liu; V J Orphan
Journal:  Geobiology       Date:  2013-06-21       Impact factor: 4.407

10.  Energy Dispersive X-ray (EDX) microanalysis: A powerful tool in biomedical research and diagnosis.

Authors:  Manuel Scimeca; Simone Bischetti; Harpreet Kaur Lamsira; Rita Bonfiglio; Elena Bonanno
Journal:  Eur J Histochem       Date:  2018-03-15       Impact factor: 3.188

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  2 in total

1.  Intracellular silicification by early-branching magnetotactic bacteria.

Authors:  Jinhua Li; Peiyu Liu; Nicolas Menguy; Xingliang Zhang; Jian Wang; Karim Benzerara; Lianjun Feng; Lei Sun; Yue Zheng; Fanqi Meng; Lin Gu; Eric Leroy; Jialong Hao; Xuelei Chu; Yongxin Pan
Journal:  Sci Adv       Date:  2022-05-13       Impact factor: 14.957

2.  Biogeochemical Niche of Magnetotactic Cocci Capable of Sequestering Large Polyphosphate Inclusions in the Anoxic Layer of the Lake Pavin Water Column.

Authors:  Cécile C Bidaud; Caroline L Monteil; Nicolas Menguy; Vincent Busigny; Didier Jézéquel; Éric Viollier; Cynthia Travert; Fériel Skouri-Panet; Karim Benzerara; Christopher T Lefevre; Élodie Duprat
Journal:  Front Microbiol       Date:  2022-01-10       Impact factor: 5.640

  2 in total

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