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Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

Ricci, Jessica N. and Coleman, Maureen L. and Welander, Paul V. and Sessions, Alex L. and Summons, Roger E. and Spear, John R. and Newman, Dianne K. (2014) Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche. ISME Journal, 8 (3). pp. 675-684. ISSN 1751-7362. PMCID PMC3930323. http://resolver.caltech.edu/CaltechAUTHORS:20140407-105009295

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Abstract

Molecular fossils of 2-methylhopanoids are prominent biomarkers in modern and ancient sediments that have been used as proxies for cyanobacteria and their main metabolism, oxygenic photosynthesis. However, substantial culture and genomic-based evidence now indicates that organisms other than cyanobacteria can make 2-methylhopanoids. Because few data directly address which organisms produce 2-methylhopanoids in the environment, we used metagenomic and clone library methods to determine the environmental diversity of hpnP, the gene encoding the C-2 hopanoid methylase. Here we show that hpnP copies from alphaproteobacteria and as yet uncultured organisms are found in diverse modern environments, including some modern habitats representative of those preserved in the rock record. In contrast, cyanobacterial hpnP genes are rarer and tend to be localized to specific habitats. To move beyond understanding the taxonomic distribution of environmental 2-methylhopanoid producers, we asked whether hpnP presence might track with particular variables. We found hpnP to be significantly correlated with organisms, metabolisms and environments known to support plant–microbe interactions (P-value<10^−6); in addition, we observed diverse hpnP types in closely packed microbial communities from other environments, including stromatolites, hot springs and hypersaline microbial mats. The common features of these niches indicate that 2-methylhopanoids are enriched in sessile microbial communities inhabiting environments low in oxygen and fixed nitrogen with high osmolarity. Our results support the earlier conclusion that 2-methylhopanoids are not reliable biomarkers for cyanobacteria or any other taxonomic group, and raise the new hypothesis that, instead, they are indicators of a specific environmental niche.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1038/ismej.2013.191DOIArticle
http://www.nature.com/ismej/journal/v8/n3/full/ismej2013191a.htmlPublisherArticle
http://www.nature.com/ismej/journal/v8/n3/suppinfo/ismej2013191s1.htmlUNSPECIFIEDSupplemental material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3930323/PubMed CentralArticle
ORCID:
AuthorORCID
Sessions, Alex L.0000-0001-6120-2763
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2014 International Society for Microbial Ecology. Received 14 July 2013; revised 4 September 2013; accepted 22 September 2013; published online 24 October 2013. We acknowledge members of the Newman lab for constructive comments on the manuscript. This work was supported by grants from the Howard Hughes Medical Institute to DKN and a NASA award (NNX12AD93G) to DKN, ALS and RES. Research access to Yellowstone hot springs was granted to JRS from the Yellowstone Center for Resources. We thank V Orphan, D Des Marais, the NASA Ames Research Center and ESSA Exportadora del Sal, SA, de CV, Guerrero Negro, Baja, California Sur, Mexico for samples of Guerrero Negro microbial mats. We are grateful to E Allen, J Valliere, D Caron and A Lie for help with sample collection. JNR was supported by an NSF graduate fellowship, MLC by an Agouron Institute postdoctoral fellowship and PVW by a NASA Astrobiology Institute postdoctoral fellowship. DKN is an HHMI Investigator.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NASANNX12AD93G
NSF Graduate Research FellowshipUNSPECIFIED
Agouron InstituteUNSPECIFIED
NASA Postdoctoral ProgramUNSPECIFIED
Subject Keywords:biomarker; 2-methylhopanoid; plant–microbe interaction
PubMed Central ID:PMC3930323
Record Number:CaltechAUTHORS:20140407-105009295
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140407-105009295
Official Citation:Ricci, J. N., Coleman, M. L., Welander, P. V., Sessions, A. L., Summons, R. E., Spear, J. R., & Newman, D. K. (2014). Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche. [Original Article]. ISME J, 8(3), 675-684. doi: 10.1038/ismej.2013.191
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:44692
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:08 Apr 2014 01:03
Last Modified:24 Oct 2017 16:21

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