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Carbon isotopic heterogeneity of coenzyme F430 and membrane lipids in methane‐oxidizing archaea

Bird, Laurence R. and Dawson, Katherine S. and Chadwick, Grayson L. and Fulton, James M. and Orphan, Victoria J. and Freeman, Katherine H. (2019) Carbon isotopic heterogeneity of coenzyme F430 and membrane lipids in methane‐oxidizing archaea. Geobiology, 17 (6). pp. 611-627. ISSN 1472-4677. https://resolver.caltech.edu/CaltechAUTHORS:20190731-105709287

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Abstract

Archaeal ANaerobic MEthanotrophs (ANME) facilitate the anaerobic oxidation of methane (AOM), a process that is believed to proceed via the reversal of the methanogenesis pathway. Carbon isotopic composition studies indicate that ANME are metabolically diverse and able to assimilate metabolites including methane, methanol, acetate, and dissolved inorganic carbon (DIC). Our data support the interpretation that ANME in marine sediments at methane seeps assimilate both methane and DIC, and the carbon isotopic compositions of the tetrapyrrole coenzyme F430 and the membrane lipids archaeol and hydroxy‐archaeol reflect their relative proportions of carbon from these substrates. Methane is assimilated via the methyl group of CH_3‐tetrahydromethanopterin (H_4MPT) and DIC from carboxylation reactions that incorporate free intracellular DIC. F430 was enriched in ^(13)C (mean δ^(13)C = −27‰ for Hydrate Ridge and −80‰ for the Santa Monica Basin) compared to the archaeal lipids (mean δ^(13)C = −97‰ for Hydrate Ridge and −122‰ for the Santa Monica Basin). We propose that depending on the side of the tricarboxylic acid (TCA) cycle used to synthesize F430, its carbon was derived from 76% DIC and 24% methane via the reductive side or 57% DIC and 43% methane via the oxidative side. ANME lipids are predicted to contain 42% DIC and 58% methane, reflecting the amount of each assimilated into acetyl‐CoA. With isotope models that include variable fractionation during biosynthesis for different carbon substrates, we show the estimated amounts of DIC and methane can result in carbon isotopic compositions of − 73‰ to − 77‰ for F430 and − 105‰ for archaeal lipids, values close to those for Santa Monica Basin. The F430 δ^(13)C value for Hydrate Ridge was 13C‐enriched compared with the modeled value, suggesting there is divergence from the predicted two carbon source models.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1111/gbi.12354DOIArticle
ORCID:
AuthorORCID
Bird, Laurence R.0000-0002-6034-9533
Dawson, Katherine S.0000-0001-8856-4609
Chadwick, Grayson L.0000-0003-0700-9350
Fulton, James M.0000-0001-7213-8015
Orphan, Victoria J.0000-0002-5374-6178
Freeman, Katherine H.0000-0002-3350-7671
Additional Information:© 2019 John Wiley & Sons Ltd. Issue Online: 18 October 2019; Version of Record online: 31 July 2019; Manuscript accepted: 23 June 2019; Manuscript revised: 17 June 2019; Manuscript received: 20 August 2018. We thank Denny Walizer and Clayton Magill for help in the Penn State Organic Geochemistry Lab and Christopher Junium and Pratigya Polissar for help with the nano‐EA‐IRMS system. Anne Dekas, Stephanie Connon, and Jennifer Glass are thanked for sample collection. We also thank Sara Lincoln for constructive comments. Fenfang Wu in the Caltech Stable Isotope facility and Nathan Daleska in the Caltech Environmental Analysis Center are thanked for providing technical assistance. Funding support for this study came from Royal Dutch Shell Geosciences Energy Research Facilitation Awards, ConocoPhillips graduate student fellowship, the Penn State Astrobiology Research Center, and Pennsylvania Space Grant, the American Chemical Society petroleum research fund (54478‐ND2). Research conducted at Caltech was funded by the Gordon and Betty Moore Foundation (Grant GBMF 3306).
Funders:
Funding AgencyGrant Number
Royal Dutch ShellUNSPECIFIED
ConocoPhillipsUNSPECIFIED
Pennsylvania State UniversityUNSPECIFIED
Pennsylvania Space Grant ConsortiumUNSPECIFIED
American Chemical Society Petroleum Research Fund54478‐ND2
Gordon and Betty Moore FoundationGBMF 3306
Subject Keywords:archaea; extremophiles; metabolism; uncultured microbes
Issue or Number:6
Record Number:CaltechAUTHORS:20190731-105709287
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190731-105709287
Official Citation:Bird, LR, Dawson, KS, Chadwick, GL, Fulton, JM, Orphan, VJ, Freeman, KH. Carbon isotopic heterogeneity of coenzyme F430 and membrane lipids in methane‐oxidizing archaea. Geobiology. 2019; 17: 611–627. https://doi.org/10.1111/gbi.12354
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:97550
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:31 Jul 2019 19:51
Last Modified:22 Oct 2019 20:45

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