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Fractionation of Hydrogen Isotopes by Sulfate- and Nitrate-Reducing Bacteria

Osburn, Magdalena R. and Dawson, Katherine S. and Fogel, Marilyn L. and Sessions, Alex L. (2016) Fractionation of Hydrogen Isotopes by Sulfate- and Nitrate-Reducing Bacteria. Frontiers in Microbiology, 7 . Art. No. 1166. ISSN 1664-302X. PMCID PMC4969296. doi:10.3389/fmicb.2016.01166. https://resolver.caltech.edu/CaltechAUTHORS:20160822-080815250

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Abstract

Hydrogen atoms from water and food are incorporated into biomass during cellular metabolism and biosynthesis, fractionating the isotopes of hydrogen—protium and deuterium—that are recorded in biomolecules. While these fractionations are often relatively constant in plants, large variations in the magnitude of fractionation are observed for many heterotrophic microbes utilizing different central metabolic pathways. The correlation between metabolism and lipid δ^2H provides a potential basis for reconstructing environmental and ecological parameters, but the calibration dataset has thus far been limited mainly to aerobes. Here we report on the hydrogen isotopic fractionations of lipids produced by nitrate-respiring and sulfate-reducing bacteria. We observe only small differences in fractionation between oxygen- and nitrate-respiring growth conditions, with a typical pattern of variation between substrates that is broadly consistent with previously described trends. In contrast, fractionation by sulfate-reducing bacteria does not vary significantly between different substrates, even when autotrophic and heterotrophic growth conditions are compared. This result is in marked contrast to previously published observations and has significant implications for the interpretation of environmental hydrogen isotope data. We evaluate these trends in light of metabolic gene content of each strain, growth rate, and potential flux and reservoir-size effects of cellular hydrogen, but find no single variable that can account for the differences between nitrate- and sulfate-respiring bacteria. The emerging picture of bacterial hydrogen isotope fractionation is therefore more complex than the simple correspondence between δ^2H and metabolic pathway previously understood from aerobes. Despite the complexity, the large signals and rich variability of observed lipid δ^2H suggest much potential as an environmental recorder of metabolism.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.3389/fmicb.2016.01166DOIArticle
http://journal.frontiersin.org/article/10.3389/fmicb.2016.01166/fullPublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4969296/PublisherArticle
ORCID:
AuthorORCID
Osburn, Magdalena R.0000-0001-9180-559X
Dawson, Katherine S.0000-0001-8856-4609
Sessions, Alex L.0000-0001-6120-2763
Additional Information:© 2016 Osburn, Dawson, Fogel and Sessions. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 10 March 2016; Accepted: 13 July 2016; Published: 02 August 2016. Author Contributions: This manuscript is part of the thesis work of MO who completed the bulk of the experiments, measurements, and writing of this manuscript. KD cultured one strain of bacteria and contributed significantly to the genetic components of the manuscript. MF contributed measurements of bulk microbial biomass that significantly shaped the arguments within the manuscript. The majority of experiments and measurements were completed in the laboratories of AS who also contributed significantly to the intellectual development of the project, advisement of MO, and formulation of the manuscript. All authors contributed to writing and editing of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank Jared Leadbetter and Victoria Orphan for initial guidance and use of laboratory facilities, the ARS culture collection for strain access, Lichun Zhang and Fenfang Wu for laboratory assistance, Sebastian Kopf for helpful discussions, and Pratixa Savalia for help culturing S. oneidensis. This research was supported by an NSF GRFP award to MO, a Penn State Astrobiology Research Center [through the NASA Astrobiology Institute (NNA09DA76A)] postdoctoral fellowship to KD, and by EAR-1529120 to AS. We thank Christina Bradley and David Araiza (UC Merced) for assistance in measuring the bulk δ^2H measurements of cultures.
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipUNSPECIFIED
NASA Postdoctoral FellowshipNNA09DA76A
NSFEAR-1529120
Subject Keywords:fatty acids, hydrogen isotopes, sulfate-reducing bacteria, anaerobic microbial metabolism, NAD(P)H, transhydrogenase
PubMed Central ID:PMC4969296
DOI:10.3389/fmicb.2016.01166
Record Number:CaltechAUTHORS:20160822-080815250
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160822-080815250
Official Citation:Osburn MR, Dawson KS, Fogel ML and Sessions AL (2016) Fractionation of Hydrogen Isotopes by Sulfate- and Nitrate-Reducing Bacteria. Front. Microbiol. 7:1166. doi: 10.3389/fmicb.2016.01166
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:69803
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:22 Aug 2016 20:54
Last Modified:11 Nov 2021 04:20

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