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Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes

Welander, Paula V. and Coleman, Maureen L. and Sessions, Alex L. and Summons, Roger E. and Newman, Dianne K. (2010) Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes. Proceedings of the National Academy of Sciences of the United States of America, 107 (19). pp. 8537-8542. ISSN 0027-8424. PMCID PMC2889317. http://resolver.caltech.edu/CaltechAUTHORS:20100601-111422016

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Abstract

The rise of atmospheric oxygen has driven environmental change and biological evolution throughout much of Earth’s history and was enabled by the evolution of oxygenic photosynthesis in the cyanobacteria. Dating this metabolic innovation using inorganic proxies from sedimentary rocks has been difficult and one important approach has been to study the distributions of fossil lipids, such as steranes and 2-methylhopanes, as biomarkers for this process. 2-methylhopanes arise from degradation of 2-methylbacteriohopanepolyols (2-MeBHPs), lipids thought to be synthesized primarily by cyanobacteria. The discovery that 2-MeBHPs are produced by an anoxygenic phototroph, however, challenged both their taxonomic link with cyanobacteria and their functional link with oxygenic photosynthesis. Here, we identify a radical SAM methylase encoded by the hpnP gene that is required for methylation at the C-2 position in hopanoids. This gene is found in several, but not all, cyanobacteria and also in α -proteobacteria and acidobacteria. Thus, one cannot extrapolate from the presence of 2-methylhopanes alone, in modern environments or ancient sedimentary rocks, to a particular taxonomic group or metabolism. To understand the origin of this gene, we reconstructed the evolutionary history of HpnP. HpnP proteins from cyanobacteria, Methylobacterium species, and other α-proteobacteria form distinct phylogenetic clusters, but the branching order of these clades could not be confidently resolved. Hence,it is unclear whether HpnP, and 2-methylhopanoids, originated first in the cyanobacteria. In summary, existing evidence does not support the use of 2-methylhopanes as biomarkers for oxygenic photosynthesis.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.0912949107DOIArticle
http://www.pnas.org/content/107/19/8537PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2889317/PubMed CentralArticle
http://www.pnas.org/cgi/content/full/0912949107/DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Sessions, Alex L.0000-0001-6120-2763
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2010 National Academy of Sciences. Edited by John M. Hayes, Woods Hole Oceanographic Institution, Berkeley, CA, and approved January 27, 2010 (received for review November 10, 2009). Published online before print April 26, 2010. We thank David Doughty, Jacob Waldbauer, and Eric Alm for technical assistance and helpful discussions, and the reviewers for their constructive comments that improved the manuscript. This work was supported by grants from the National Aeronautics and Space Administration (NASA) Exobiology Program (A.L.S., D.K.N., and R.E.S.), the NASA Astrobiology Institute (R.E.S), a National Science Foundation Postdoctoral Minority Fellowship (P.V.W.), and an Agouron Institute Geobiology Postdoctoral Fellowship (M.L.C.). D.K.N. is an Investigator of The Howard Hughes Medical Institute. P.V.W and M.L.C. contributed equally to this work. Author contributions: P.V.W., M.L.C., and D.K.N. designed research; P.V.W. and M.L.C. performed research; A.L.S. and R.E.S. contributed new reagents/analytic tools; P.V.W., M.L.C., A.L.S., R.E.S., and D.K.N. analyzed data; and P.V.W., M.L.C., and D.K.N. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/cgi/content/full/0912949107/DCSupplemental.
Funders:
Funding AgencyGrant Number
NASAUNSPECIFIED
NSF Postdoctoral Minority FellowshipUNSPECIFIED
Agouron InstituteUNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:biomarkers; cyanobacteria; hopanoids; phylogeny; radical SAM
PubMed Central ID:PMC2889317
Record Number:CaltechAUTHORS:20100601-111422016
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20100601-111422016
Official Citation:Paula V. Welander, Maureen L. Coleman, Alex L. Sessions, Roger E. Summons, and Dianne K. Newman Identification of a methylase required for 2-methylhopanoid production and implications for the interpretation of sedimentary hopanes PNAS 2010 107 (19) 8537-8542; published ahead of print April 26, 2010, doi:10.1073/pnas.0912949107
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:18503
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:02 Jun 2010 18:13
Last Modified:24 Oct 2017 15:56

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