Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes

Magnetotactic bacteria (MTB) are morphologically and phylogenetically diverse prokaryotes. They can form intracellular chain-assembled magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals each enveloped by a lipid bilayer membrane called a magnetosome. Magnetotactic cocci have been found to be the mos...

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Main Authors: Heng Zhang, Nicolas Menguy, Fuxian Wang, Karim Benzerara, Eric Leroy, Peiyu Liu, Wenqi Liu, Chunli Wang, Yongxin Pan, Zhibao Chen, Jinhua Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-05-01
Series:Frontiers in Microbiology
Subjects:
TEM
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.00969/full
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language English
format Article
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author Heng Zhang
Heng Zhang
Heng Zhang
Heng Zhang
Nicolas Menguy
Nicolas Menguy
Fuxian Wang
Fuxian Wang
Fuxian Wang
Karim Benzerara
Eric Leroy
Peiyu Liu
Peiyu Liu
Peiyu Liu
Wenqi Liu
Wenqi Liu
Wenqi Liu
Chunli Wang
Yongxin Pan
Yongxin Pan
Zhibao Chen
Jinhua Li
Jinhua Li
Jinhua Li
spellingShingle Heng Zhang
Heng Zhang
Heng Zhang
Heng Zhang
Nicolas Menguy
Nicolas Menguy
Fuxian Wang
Fuxian Wang
Fuxian Wang
Karim Benzerara
Eric Leroy
Peiyu Liu
Peiyu Liu
Peiyu Liu
Wenqi Liu
Wenqi Liu
Wenqi Liu
Chunli Wang
Yongxin Pan
Yongxin Pan
Zhibao Chen
Jinhua Li
Jinhua Li
Jinhua Li
Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
Frontiers in Microbiology
magnetotactic cocci
magnetosome
biomineralization
octahedron
coordinated FISH-SEM
TEM
author_facet Heng Zhang
Heng Zhang
Heng Zhang
Heng Zhang
Nicolas Menguy
Nicolas Menguy
Fuxian Wang
Fuxian Wang
Fuxian Wang
Karim Benzerara
Eric Leroy
Peiyu Liu
Peiyu Liu
Peiyu Liu
Wenqi Liu
Wenqi Liu
Wenqi Liu
Chunli Wang
Yongxin Pan
Yongxin Pan
Zhibao Chen
Jinhua Li
Jinhua Li
Jinhua Li
author_sort Heng Zhang
title Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
title_short Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
title_full Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
title_fullStr Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
title_full_unstemmed Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite Magnetosomes
title_sort magnetotactic coccus strain shhc-1 affiliated to alphaproteobacteria forms octahedral magnetite magnetosomes
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-05-01
description Magnetotactic bacteria (MTB) are morphologically and phylogenetically diverse prokaryotes. They can form intracellular chain-assembled magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals each enveloped by a lipid bilayer membrane called a magnetosome. Magnetotactic cocci have been found to be the most abundant morphotypes of MTB in various aquatic environments. However, knowledge on magnetosome biomineralization within magnetotactic cocci remains elusive due to small number of strains that have been cultured. By using a coordinated fluorescence and scanning electron microscopy method, we discovered a unique magnetotactic coccus strain (tentatively named SHHC-1) in brackish sediments collected from the estuary of Shihe River in Qinhuangdao city, eastern China. It phylogenetically belongs to the Alphaproteobacteria class. Transmission electron microscopy analyses reveal that SHHC-1 cells formed many magnetite-type magnetosomes organized as two bundles in each cell. Each bundle contains two parallel chains with smaller magnetosomes generally located at the ends of each chain. Unlike most magnetotactic alphaproteobacteria that generally form magnetosomes with uniform crystal morphologies, SHHC-1 magnetosomes display a more diverse variety of crystal morphology even within a single cell. Most particles have rectangular and rhomboidal projections, whilst others are triangular, or irregular. High resolution transmission electron microscopy observations coupled with morphological modeling indicate an idealized model—elongated octahedral crystals, a form composed of eight {111} faces. Furthermore, twins, multiple twins and stack dislocations are frequently observed in the SHHC-1 magnetosomes. This suggests that biomineralization of strain SHHC-1 magnetosome might be less biologically controlled than other magnetotactic alphaproteobacteria. Alternatively, SHHC-1 is more sensitive to the unfavorable environments under which it lives, or a combination of both factors may have controlled the magnetosome biomineralization process within this unique MTB.
topic magnetotactic cocci
magnetosome
biomineralization
octahedron
coordinated FISH-SEM
TEM
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.00969/full
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spelling doaj-ca05580816c94afe856c9901870c84912020-11-24T22:37:18ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-05-01810.3389/fmicb.2017.00969247644Magnetotactic Coccus Strain SHHC-1 Affiliated to Alphaproteobacteria Forms Octahedral Magnetite MagnetosomesHeng Zhang0Heng Zhang1Heng Zhang2Heng Zhang3Nicolas Menguy4Nicolas Menguy5Fuxian Wang6Fuxian Wang7Fuxian Wang8Karim Benzerara9Eric Leroy10Peiyu Liu11Peiyu Liu12Peiyu Liu13Wenqi Liu14Wenqi Liu15Wenqi Liu16Chunli Wang17Yongxin Pan18Yongxin Pan19Zhibao Chen20Jinhua Li21Jinhua Li22Jinhua Li23Department of Life Science and Technology, Heilongjiang Bayi Agricultural UniversityDaqing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Marine Geology, Qingdao National Laboratory for Marine Science and TechnologyQingdao, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaIMPMC, Centre National de la Recherche Scientifique, UMR 7590, Sorbonne Universités, MNHN, UPMC, IRD UMR 206Paris, FranceKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Marine Geology, Qingdao National Laboratory for Marine Science and TechnologyQingdao, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaIMPMC, Centre National de la Recherche Scientifique, UMR 7590, Sorbonne Universités, MNHN, UPMC, IRD UMR 206Paris, FranceFrance Chimie Me′tallurgique des Terres Rares, ICMPE, UMR 7182, Centre National de la Recherche ScientifiqueThiais, FranceKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Marine Geology, Qingdao National Laboratory for Marine Science and TechnologyQingdao, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Marine Geology, Qingdao National Laboratory for Marine Science and TechnologyQingdao, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaDepartment of Life Science and Technology, Heilongjiang Bayi Agricultural UniversityDaqing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaDepartment of Life Science and Technology, Heilongjiang Bayi Agricultural UniversityDaqing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Marine Geology, Qingdao National Laboratory for Marine Science and TechnologyQingdao, ChinaFrance-China Biomineralization and Nano-structures Laboratory, Chinese Academy of SciencesBeijing, ChinaMagnetotactic bacteria (MTB) are morphologically and phylogenetically diverse prokaryotes. They can form intracellular chain-assembled magnetite (Fe3O4) or greigite (Fe3S4) nanocrystals each enveloped by a lipid bilayer membrane called a magnetosome. Magnetotactic cocci have been found to be the most abundant morphotypes of MTB in various aquatic environments. However, knowledge on magnetosome biomineralization within magnetotactic cocci remains elusive due to small number of strains that have been cultured. By using a coordinated fluorescence and scanning electron microscopy method, we discovered a unique magnetotactic coccus strain (tentatively named SHHC-1) in brackish sediments collected from the estuary of Shihe River in Qinhuangdao city, eastern China. It phylogenetically belongs to the Alphaproteobacteria class. Transmission electron microscopy analyses reveal that SHHC-1 cells formed many magnetite-type magnetosomes organized as two bundles in each cell. Each bundle contains two parallel chains with smaller magnetosomes generally located at the ends of each chain. Unlike most magnetotactic alphaproteobacteria that generally form magnetosomes with uniform crystal morphologies, SHHC-1 magnetosomes display a more diverse variety of crystal morphology even within a single cell. Most particles have rectangular and rhomboidal projections, whilst others are triangular, or irregular. High resolution transmission electron microscopy observations coupled with morphological modeling indicate an idealized model—elongated octahedral crystals, a form composed of eight {111} faces. Furthermore, twins, multiple twins and stack dislocations are frequently observed in the SHHC-1 magnetosomes. This suggests that biomineralization of strain SHHC-1 magnetosome might be less biologically controlled than other magnetotactic alphaproteobacteria. Alternatively, SHHC-1 is more sensitive to the unfavorable environments under which it lives, or a combination of both factors may have controlled the magnetosome biomineralization process within this unique MTB.http://journal.frontiersin.org/article/10.3389/fmicb.2017.00969/fullmagnetotactic coccimagnetosomebiomineralizationoctahedroncoordinated FISH-SEMTEM