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Metabolic associations with archaea drive shifts in hydrogen isotope fractionation in sulfate-reducing bacterial lipids in cocultures and methane seeps

Dawson, K. S. and Osburn, M. R. and Sessions, A. L. and Orphan, V. J. (2015) Metabolic associations with archaea drive shifts in hydrogen isotope fractionation in sulfate-reducing bacterial lipids in cocultures and methane seeps. Geobiology, 13 (5). pp. 462-477. ISSN 1472-4677. https://resolver.caltech.edu/CaltechAUTHORS:20150505-105030332

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Abstract

Correlation between hydrogen isotope fractionation in fatty acids and carbon metabolism in pure cultures of bacteria indicates the potential of biomarker D/H analysis as a tool for diagnosing carbon substrate usage in environmental samples. However, most environments, in particular anaerobic habitats, are built from metabolic networks of micro-organisms rather than a single organism. The effect of these networks on D/H of lipids has not been explored and may complicate the interpretation of these analyses. Syntrophy represents an extreme example of metabolic interdependence. Here, we analyzed the effect of metabolic interactions on the D/H biosignatures of sulfate-reducing bacteria (SRB) using both laboratory maintained cocultures of the methanogen Methanosarcina acetivorans and the SRB Desulfococcus multivorans in addition to environmental samples harboring uncultured syntrophic consortia of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing Deltaproteobacteria (SRB) recovered from deep-sea methane seeps. Consistent with previously reported trends, we observed a ~80‰ range in hydrogen isotope fractionation (ε_(lipid–water)) for D. multivorans grown under different carbon assimilation conditions, with more D-enriched values associated with heterotrophic growth. In contrast, for cocultures of D. multivorans with M. acetivorans, we observed a reduced range of ε_(lipid–water) values (~36‰) across substrates with shifts of up to 61‰ compared to monocultures. Sediment cores from methane seep settings in Hydrate Ridge (offshore Oregon, USA) showed similar D-enrichment in diagnostic SRB fatty acids coinciding with peaks in ANME/SRB consortia concentration suggesting that metabolic associations are connected to the observed shifts in ε_(lipid–water) values.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/gbi.12140DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/gbi.12140/abstractPublisherArticle
http://onlinelibrary.wiley.com/doi/10.1111/gbi.12140/suppinfoRelated ItemSupporting Information
ORCID:
AuthorORCID
Dawson, K. S.0000-0001-8856-4609
Osburn, M. R.0000-0001-9180-559X
Sessions, A. L.0000-0001-6120-2763
Orphan, V. J.0000-0002-5374-6178
Additional Information:© 2015 John Wiley & Sons Ltd. Received 4 November 2014; accepted 30 March 2015. Article first published online: 28 Apr 2015. We thank the shipboard, scientific crew and pilots of the R/V Atlantis and DSV Jason. Stephanie Connon, Fenfang Wu, and Lichun Zhang provided technical assistance. Laurence Bird and Katherine Freeman provided the ^(13)C_(lipid) measurements. We would also like to thank four anonymous reviewers for their comments toward improving this manuscript. This study was supported by a grant from the Penn State Astrobiology Research Centre (through the NASA Astrobiology Institute (NNA09DA76A)) to VJO, a PSARC post-doctoral fellowship to KSD and an NSF Graduate Fellowship to MRO. Additional support was provided by the Gordon and Betty Moore Foundation Marine Microbiology Initiative (grant #3780) and an early career grant from the U.S. Department of Energy, Office of Biological and Environmental Research to VJO.
Funders:
Funding AgencyGrant Number
NASANNA09DA76A
Penn State Astrobiology Research Center (PSARC)UNSPECIFIED
NSF Graduate FellowshipUNSPECIFIED
Gordon and Betty Moore Foundation3780
Department of Energy (DOE)UNSPECIFIED
Issue or Number:5
Record Number:CaltechAUTHORS:20150505-105030332
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150505-105030332
Official Citation:Dawson, K. S., Osburn, M. R., Sessions, A. L. and Orphan, V. J. (2015), Metabolic associations with archaea drive shifts in hydrogen isotope fractionation in sulfate-reducing bacterial lipids in cocultures and methane seeps. Geobiology, 13: 462–477. doi: 10.1111/gbi.12140
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:57229
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:05 May 2015 19:25
Last Modified:03 Oct 2019 08:22

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