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Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme

Ricci, J. N. and Morton, R. and Kulkarni, G. and Summers, M. L. and Newman, D. K. (2017) Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme. Geobiology, 15 (1). pp. 173-183. ISSN 1472-4677. http://resolver.caltech.edu/CaltechAUTHORS:20160822-074307063

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Abstract

Hopanes are abundant in ancient sedimentary rocks at discrete intervals in Earth history, yet interpreting their significance in the geologic record is complicated by our incomplete knowledge of what their progenitors, hopanoids, do in modern cells. To date, few studies have addressed the breadth of diversity of physiological functions of these lipids and whether those functions are conserved across the hopanoid-producing bacterial phyla. Here, we generated mutants in the filamentous cyanobacterium, Nostoc punctiforme, that are unable to make all hopanoids (shc) or 2-methylhopanoids (hpnP). While the absence of hopanoids impedes growth of vegetative cells at high temperature, the shc mutant grows faster at low temperature. This finding is consistent with hopanoids acting as membrane rigidifiers, a function shared by other hopanoid-producing phyla. Apart from impacting fitness under temperature stress, hopanoids are dispensable for vegetative cells under other stress conditions. However, hopanoids are required for stress tolerance in akinetes, a resting survival cell type. While 2-methylated hopanoids do not appear to contribute to any stress phenotype, total hopanoids and to a lesser extent 2-methylhopanoids were found to promote the formation of cyanophycin granules in akinetes. Finally, although hopanoids support symbiotic interactions between Alphaproteobacteria and plants, they do not appear to facilitate symbiosis between N. punctiforme and the hornwort Anthoceros punctatus. Collectively, these findings support interpreting hopanes as general environmental stress biomarkers. If hopanoid-mediated enhancement of nitrogen-rich storage products turns out to be a conserved phenomenon in other organisms, a better understanding of this relationship may help us parse the enrichment of 2-methylhopanes in the rock record during episodes of disrupted nutrient cycling.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/gbi.12204DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/gbi.12204/abstractPublisherArticle
ORCID:
AuthorORCID
Newman, D. K.0000-0003-1647-1918
Additional Information:© 2016 John Wiley & Sons Ltd. Received: 19 February 2016; Accepted: 15 July 2016; First published: 16 August 2016. We thank Caj Neubauer and Chia-Hung Wu for helpful discussions and assistance with LC-MS and GC-MS. We are grateful to Jack Meeks and Elsie Campbell for their help with N. punctiforme mutant construction and A. punctatus. The manuscript improved significantly thanks to constructive feedback from Ann Pearson and two anonymous reviewers. This work was supported by grants from NASA (NNX12AD93G), the National Science Foundation (1224158), and the Howard Hughes Medical Institute to DKN as well as NSF grant MCB-1413583 and NIH grant 1SC1 GM093998 to MLS. JNR was supported by an NSF graduate fellowship. DKN is an Investigator of the Howard Hughes Medical Institute.
Funders:
Funding AgencyGrant Number
NASANNX12AD93G
NSFCHE-1224158
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NSFMCB-1413583
NIH1SC1 GM093998
NSF Graduate Research FellowshipUNSPECIFIED
Record Number:CaltechAUTHORS:20160822-074307063
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160822-074307063
Official Citation:Ricci, J. N., Morton, R., Kulkarni, G., Summers, M. L. and Newman, D. K. (2017), Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme. Geobiology, 15: 173–183. doi:10.1111/gbi.12204
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:69802
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:22 Aug 2016 21:01
Last Modified:24 Oct 2017 16:46

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