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Polyphosphate Storage during Sporulation in the Gram-Negative Bacterium Acetonema longum

Tocheva, Elitza I. and Dekas, Anne E. and McGlynn, Shawn E. and Morris, Dylan and Orphan, Victoria J. and Jensen, Grant J. (2013) Polyphosphate Storage during Sporulation in the Gram-Negative Bacterium Acetonema longum. Journal of Bacteriology, 195 (17). pp. 3940-3946. ISSN 0021-9193. PMCID PMC3754598. http://resolver.caltech.edu/CaltechAUTHORS:20130909-141442695

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Abstract

Using electron cryotomography, we show that the Gram-negative sporulating bacterium Acetonema longum synthesizes high-density storage granules at the leading edges of engulfing membranes. The granules appear in the prespore and increase in size and number as engulfment proceeds. Typically, a cluster of 8 to 12 storage granules closely associates with the inner spore membrane and ultimately accounts for ∼7% of the total volume in mature spores. Energy-dispersive X-ray spectroscopy (EDX) analyses show that the granules contain high levels of phosphorus, oxygen, and magnesium and therefore are likely composed of polyphosphate (poly-P). Unlike the Gram-positive Bacilli and Clostridia, A. longum spores retain their outer spore membrane upon germination. To explore the possibility that the granules in A. longum may be involved in this unique process, we imaged purified Bacillus cereus, Bacillus thuringiensis, Bacillus subtilis, and Clostridium sporogenes spores. Even though B. cereus and B. thuringiensis contain the ppk and ppx genes, none of the spores from Gram-positive bacteria had granules. We speculate that poly-P in A. longum may provide either the energy or phosphate metabolites needed for outgrowth while retaining an outer membrane.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1128/JB.00712-13 DOIArticle
http://jb.asm.org/content/195/17/3940PublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3754598/PubMed CentralArticle
ORCID:
AuthorORCID
Tocheva, Elitza I.0000-0002-4869-8319
Orphan, Victoria J.0000-0002-5374-6178
Jensen, Grant J.0000-0003-1556-4864
Additional Information:© 2013 American Society for Microbiology. Received 16 June 2013 Accepted 20 June 2013; Published ahead of print 28 June 2013. We acknowledge the use of electron microscopy facilities at the UCLA Electron Imaging Center for NanoMachines at the California NanoSystems Institute (CNSI) and thank Ivo Atanasov and Dan Taso for technical assistance with EDX data collection and analysis. We thank Yunbin Guan and John Eiler for assistance with the NanoSIMS measurements. We thank Adrian Ponce for providing the C. sporogenes spores. The NanoSIMS apparatus is housed within the Caltech Microanalysis Center and is partially funded by the Gordon and Betty Moore Foundation. This work was funded in part by the Howard Hughes Medical Institute, the Caltech Center for Environmental Microbial Interactions, and gifts to Caltech from the Gordon and Betty Moore Foundation. This work was partially performed under the auspices of the U.S. Department of Energy by Lawrence Livermore National Laboratory under contract DE-AC52-07NA27344.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Department of Energy (DOE)DE-AC52-07NA27344
PubMed Central ID:PMC3754598
Record Number:CaltechAUTHORS:20130909-141442695
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20130909-141442695
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:41193
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:16 Sep 2013 21:35
Last Modified:20 Oct 2017 20:17

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