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Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti

Tavormina, Patricia L. and Kellermann, Matthias Y. and Antony, Chakkiath Paul and Tocheva, Elitza I. and Dalleska, Nathan F. and Jensen, Ashley J. and Valentine, David L. and Hinrichs, Kai-Uwe and Jensen, Grant J. and Dubilier, Nicole and Orphan, Victoria J. (2017) Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti. Molecular Microbiology, 103 (2). pp. 242-252. ISSN 0950-382X. http://resolver.caltech.edu/CaltechAUTHORS:20161017-155437081

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Abstract

In the deep ocean, the conversion of methane into derived carbon and energy drives the establishment of diverse faunal communities. Yet specific biological mechanisms underlying the introduction of methane-derived carbon into the food web remain poorly described, due to a lack of cultured representative deep-sea methanotrophic prokaryotes. Here, the response of the deep-sea aerobic methanotroph Methyloprofundus sedimenti to methane starvation and recovery was characterized. By combining lipid analysis, RNA analysis, and electron cryotomography, it was shown that M. sedimenti undergoes discrete cellular shifts in response to methane starvation, including changes in headgroup-specific fatty acid saturation levels, and reductions in cytoplasmic storage granules. Methane starvation is associated with a significant increase in the abundance of gene transcripts pertinent to methane oxidation. Methane reintroduction to starved cells stimulates a rapid, transient extracellular accumulation of methanol, revealing a way in which methane-derived carbon may be routed to community members. This study provides new understanding of methanotrophic responses to methane starvation and recovery, and lays the initial groundwork to develop Methyloprofundus as a model chemosynthesizing bacterium from the deep sea.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/mmi.13553DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/mmi.13553/abstractPublisherArticle
ORCID:
AuthorORCID
Dalleska, Nathan F.0000-0002-2059-1587
Hinrichs, Kai-Uwe0000-0002-0739-9291
Jensen, Grant J.0000-0003-1556-4864
Dubilier, Nicole0000-0002-9394-825X
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2016 John Wiley & Sons Ltd. Issue online: 6 January 2017; Version of record online: 22 November 2016; Accepted manuscript online: 14 October 2016; Manuscript Accepted: 8 October 2016. GC-FID measurements were performed in the Environmental Analysis Center at Caltech. We thank Paul Magyar for assistance with GC-FID, and Songye Chen for assistance segmenting crytomographic files. Special thanks for electron microscopy support from Dr. Alasdair McDowall, Howard Hughes Medical Institute. The Caltech electron microscopy facility is supported in part by the Gordon and Betty Moore Foundation, the Agouron Institute and the Beckman Foundation. Funding for this work was provided by the Gordon and Betty Moore Foundation (GBMF3780, VJO; GBMF3811, ND) and the National Science Foundation (OCE-1046144, DLV; EAR-0950600, MYK).
Funders:
Funding AgencyGrant Number
Agouron InstituteUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Gordon and Betty Moore FoundationGBMF3780
Gordon and Betty Moore FoundationGBMF3811
NSFOCE-1046144
NSFEAR-0950600
Record Number:CaltechAUTHORS:20161017-155437081
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20161017-155437081
Official Citation:Tavormina, P. L., Kellermann, M. Y., Antony, C. P., Tocheva, E. I., Dalleska, N. F., Jensen, A. J., Valentine, D. L., Hinrichs, K.-U., Jensen, G. J., Dubilier, N. and Orphan, V. J. (2017), Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti. Molecular Microbiology, 103: 242–252. doi:10.1111/mmi.13553
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:71196
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 Oct 2016 23:55
Last Modified:29 Mar 2017 21:57

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