Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme
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.
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.Attached Files
Supplemental Material - gbi12204-sup-0001-FigS1.pdf
Supplemental Material - gbi12204-sup-0002-FigS2.pdf
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Additional details
- Eprint ID
- 69802
- Resolver ID
- CaltechAUTHORS:20160822-074307063
- NASA
- NNX12AD93G
- NSF
- CHE-1224158
- Howard Hughes Medical Institute (HHMI)
- NSF
- MCB-1413583
- NIH
- 1SC1 GM093998
- NSF Graduate Research Fellowship
- Created
-
2016-08-22Created from EPrint's datestamp field
- Updated
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2021-11-11Created from EPrint's last_modified field
- Caltech groups
- Division of Geological and Planetary Sciences