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

Cornejo, Elias and Subramanian, Poorna and Li, Zhuo and Jensen, Grant J. and Komeili, Arash (2016) Dynamic Remodeling of the Magnetosome Membrane Is Triggered by the Initiation of Biomineralization. mBio, 7 (1). e01898-15. ISSN 2150-7511. PMCID PMC4791847. doi:10.1128/mBio.01898-15. https://resolver.caltech.edu/CaltechAUTHORS:20160222-140321490

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1128/mBio.01898-15 DOIArticle
http://mbio.asm.org/content/7/1/e01898-15.fullPublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4791847/PubMed CentralArticle
ORCID:
AuthorORCID
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2016 Cornejo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Received 2 November 2015. Accepted 20 January 2016. Published 16 February 2016. Editor Yves V. Brun, Indiana University. We thank Dorothée Murat for her intellectual contributions and outstanding mentorship during the early stages of this project. National Science Foundation (NSF) provided funding to Elias Cornejo under grant number DGE 110640. HHS | NIH | National Institute of General Medical Sciences (NIGMS) provided funding to Elias Cornejo and Arash Komeili under grant number R01GM084122. Howard Hughes Medical Institute (HHMI) provided funding to Poorna Subramanian, Zhuo Li, and Grant J. Jensen. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipDGE-1106400
NIHR01GM084122
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Issue or Number:1
PubMed Central ID:PMC4791847
DOI:10.1128/mBio.01898-15
Record Number:CaltechAUTHORS:20160222-140321490
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160222-140321490
Official Citation:Cornejo E, Subramanian P, Li Z, Jensen G, Komeili A. 2016. Dynamic remodeling of the magnetosome membrane is triggered by the initiation of biomineralization. mBio 7(1):e01898-15. doi:10.1128/mBio.01898-15.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:64641
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:22 Feb 2016 23:10
Last Modified:10 Nov 2021 23:33

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