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CO_2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway

Pearson, Ann and Hurley, Sarah J. and Elling, Felix J. and Wilkes, Elise B. (2019) CO_2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway. Geochimica et Cosmochimica Acta, 261 . pp. 368-382. ISSN 0016-7037. https://resolver.caltech.edu/CaltechAUTHORS:20190712-094842800

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Abstract

The 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) pathway of carbon fixation is found in thermophilic Crenarchaeota of the order Sulfolobales and in aerobic, ammonia-oxidizing Thaumarchaeota. Unlike all other known autotrophic carbon metabolisms, this pathway exclusively uses HCO_3- rather than CO_2 as the substrate for carbon fixation. Biomass produced by the 3HB/4HP pathway is relatively ^(13)C-enriched compared to biomass fixed by other autotrophic pathways, with total biosynthetic isotope effects (ε_(Ar)) of ca. 3‰ in the Sulfolobales and ca. 20‰ in the Thaumarchaeota. Explanations for the difference between these values usually invoke the dual effects of thermophily and growth at low pH (low [HCO_3-]) for the former group vs. mesophily and growth at pH > 7 (high [HCO_3-]) for the latter group. Here we examine the model taxa Metallosphaera sedula and Nitrosopumilus maritimususing an isotope flux-balance model to argue that the primary cause of different ε_(Ar) values more likely is the presence of carbonic anhydrase in M. sedula and its corresponding absence in N. maritimus. The results suggest that the pool of HCO_3-inside N. maritimus is out of isotopic equilibrium with CO_2 and that the organism imports < 10% HCO_3- from the extracellular environment. If correct and generalizable, the aerobic, ammonia-oxidizing marine Thaumarchaeota are dependent on passive CO_2 uptake and a slow rate of intracellular conversion to HCO_3-. Values of ε_(Ar) should therefore vary in response to growth rate (μ) and CO_2 availability, analogous to eukaryotic algae, but in the opposite direction: ε_(Ar) becomes smaller as [CO_(2(aq))] increases and/or μ decreases. Such an idea represents a testable hypothesis, both in the laboratory and in natural systems. Sensitivity to μ and CO_2 implies that measurements of ε_(Ar) may hold promise as a pCO_2 paleobarometer.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.gca.2019.06.042DOIArticle
ORCID:
AuthorORCID
Pearson, Ann0000-0003-2785-8405
Hurley, Sarah J.0000-0002-4663-4063
Elling, Felix J.0000-0003-0405-4033
Wilkes, Elise B.0000-0002-3379-7832
Alternate Title:CO2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway
Additional Information:© 2019 Elsevier Ltd. Received 23 December 2018, Revised 29 May 2019, Accepted 19 June 2019, Available online 12 July 2019. We thank Martin Könneke, Jed Fuhrman, David Johnston, Emma Bertran, Itay Halevy, Rich Pancost, and Anne Dekas for valuable discussions. We are grateful to Joe Werne for editorial assistance and to three anonymous reviewers for their valuable comments. Funding from NSF-1129343, NSF-1702262, and the Gordon and Betty Moore Foundation (to A.P.); from National Science Foundation Graduate Research Fellowship DGE-1144152 (to E.B.W.); and from the Agouron Institute (to S.J.H.) supported this work.
Funders:
Funding AgencyGrant Number
NSFOCE-1129343
NSFOCE-1702262
Gordon and Betty Moore FoundationUNSPECIFIED
NSF Graduate Research FellowshipDGE-1144152
Agouron InstituteUNSPECIFIED
Record Number:CaltechAUTHORS:20190712-094842800
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190712-094842800
Official Citation:Ann Pearson, Sarah J. Hurley, Felix J. Elling, Elise B. Wilkes, CO2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway, Geochimica et Cosmochimica Acta, Volume 261, 2019, Pages 368-382, ISSN 0016-7037, https://doi.org/10.1016/j.gca.2019.06.042. (http://www.sciencedirect.com/science/article/pii/S0016703719303916)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:97089
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:12 Jul 2019 16:57
Last Modified:03 Oct 2019 21:28

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