Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization

ABSTRACT Magnetotactic bacteria produce chains of membrane-bound organelles that direct the biomineralization of magnetic nanoparticles. These magnetosome compartments are a model for studying the biogenesis and subcellular organization of bacterial organelles. Previous studies have suggested that d...

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Autores principales:	Elias Cornejo, Poorna Subramanian, Zhuo Li, Grant J. Jensen, Arash Komeili
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/57cfbc6821674d919f3dbee41efe0751
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spelling	oai:doaj.org-article:57cfbc6821674d919f3dbee41efe07512021-11-15T15:49:40ZDynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization10.1128/mBio.01898-152150-7511https://doaj.org/article/57cfbc6821674d919f3dbee41efe07512016-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01898-15https://doaj.org/toc/2150-7511ABSTRACT Magnetotactic bacteria produce chains of membrane-bound organelles that direct the biomineralization of magnetic nanoparticles. These magnetosome compartments are a model for studying the biogenesis and subcellular organization of bacterial organelles. Previous studies have suggested that discrete gene products build and assemble magnetosomes in a stepwise fashion. Here, using an inducible system, we show that the stages of magnetosome formation are highly dynamic and interconnected. During de novo formation, magnetosomes first organize into discontinuous chain fragments that are subsequently connected by the bacterial actin-like protein MamK. We also find that magnetosome membranes are not uniform in size and can grow in a biomineralization-dependent manner. In the absence of biomineralization, magnetosome membranes stall at a diameter of ~50 nm. Those that have initiated biomineralization then expand to significantly larger sizes and accommodate mature magnetic particles. We speculate that such a biomineralization-dependent checkpoint for membrane growth establishes the appropriate conditions within the magnetosome to ensure successful nucleation and growth of magnetic particles. IMPORTANCE Magnetotactic bacteria make magnetic nanoparticles inside membrane-bound organelles called magnetosomes; however, it is unclear how the magnetosome membrane controls the biomineralization that occurs within this bacterial organelle. We placed magnetosome formation under inducible control in Magnetospirillum magneticum AMB-1 and used electron cryo-tomography to capture magnetosomes in their near-native state as they form de novo. An inducible system provided the key evidence that magnetosome membranes grow continuously unless they have not properly initiated biomineralization. Our finding that the size of a bacterial organelle impacts its biochemical function is a fundamental advance that impacts our perception of organelle formation and can inform future attempts aimed at creating designer magnetic particles.Elias CornejoPoorna SubramanianZhuo LiGrant J. JensenArash KomeiliAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 1 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Elias Cornejo Poorna Subramanian Zhuo Li Grant J. Jensen Arash Komeili Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
description	ABSTRACT Magnetotactic bacteria produce chains of membrane-bound organelles that direct the biomineralization of magnetic nanoparticles. These magnetosome compartments are a model for studying the biogenesis and subcellular organization of bacterial organelles. Previous studies have suggested that discrete gene products build and assemble magnetosomes in a stepwise fashion. Here, using an inducible system, we show that the stages of magnetosome formation are highly dynamic and interconnected. During de novo formation, magnetosomes first organize into discontinuous chain fragments that are subsequently connected by the bacterial actin-like protein MamK. We also find that magnetosome membranes are not uniform in size and can grow in a biomineralization-dependent manner. In the absence of biomineralization, magnetosome membranes stall at a diameter of ~50 nm. Those that have initiated biomineralization then expand to significantly larger sizes and accommodate mature magnetic particles. We speculate that such a biomineralization-dependent checkpoint for membrane growth establishes the appropriate conditions within the magnetosome to ensure successful nucleation and growth of magnetic particles. IMPORTANCE Magnetotactic bacteria make magnetic nanoparticles inside membrane-bound organelles called magnetosomes; however, it is unclear how the magnetosome membrane controls the biomineralization that occurs within this bacterial organelle. We placed magnetosome formation under inducible control in Magnetospirillum magneticum AMB-1 and used electron cryo-tomography to capture magnetosomes in their near-native state as they form de novo. An inducible system provided the key evidence that magnetosome membranes grow continuously unless they have not properly initiated biomineralization. Our finding that the size of a bacterial organelle impacts its biochemical function is a fundamental advance that impacts our perception of organelle formation and can inform future attempts aimed at creating designer magnetic particles.
format	article
author	Elias Cornejo Poorna Subramanian Zhuo Li Grant J. Jensen Arash Komeili
author_facet	Elias Cornejo Poorna Subramanian Zhuo Li Grant J. Jensen Arash Komeili
author_sort	Elias Cornejo
title	Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
title_short	Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
title_full	Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
title_fullStr	Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
title_full_unstemmed	Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization
title_sort	dynamic remodeling of the magnetosome membrane is triggered by the initiation of biomineralization
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/57cfbc6821674d919f3dbee41efe0751
work_keys_str_mv	AT eliascornejo dynamicremodelingofthemagnetosomemembraneistriggeredbytheinitiationofbiomineralization AT poornasubramanian dynamicremodelingofthemagnetosomemembraneistriggeredbytheinitiationofbiomineralization AT zhuoli dynamicremodelingofthemagnetosomemembraneistriggeredbytheinitiationofbiomineralization AT grantjjensen dynamicremodelingofthemagnetosomemembraneistriggeredbytheinitiationofbiomineralization AT arashkomeili dynamicremodelingofthemagnetosomemembraneistriggeredbytheinitiationofbiomineralization
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Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization

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