Stable carbon isotope ratios of intact GDGTs indicate heterogeneous sources to marine sediments

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Abstract

Thaumarchaeota, the major sources of marine glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), are believed to fix the majority of their carbon directly from dissolved inorganic carbon (DIC). The δ13C values of GDGTs (δ13CGDGT) may be powerful tools for reconstructing variations in the ocean carbon cycle, including paleoproductivity and water mass circulation, if they can be related to values of δ13CDIC. To date, isotope measurements primarily are made on the C40 biphytane skeletons of GDGTs, rather than on complete tetraether structures. This approach erases information revealed by the isotopic heterogeneity of GDGTs within a sample and may impart an isotopic fractionation associated with the ether cleavage. To circumvent these issues, we present δ13C values for GDGTs from twelve recent sediments representing ten continental margin locations. Samples are purified by orthogonal dimensions of HPLC, followed by measurement of δ13C values by Spooling Wire Microcombustion (SWiM)-isotope ratio mass spectrometry (IRMS) with 1σ precision and accuracy of ±0.25‰. Using this approach, we confirm that GDGTs, generally around −19‰, are isotopically “heavy” compared to other marine lipids. However, measured δ13CGDGT values are inconsistent with predicted values based on the 13C content of DIC in the overlying water column and the previously-published biosynthetic isotope fractionation for a pure culture of an autotrophic marine thaumarchaeon. In some sediments, the isotopic composition of individual GDGTs differs, indicating multiple source inputs. The data appear to confirm that crenarchaeol primarily is a biomarker for Thaumarchaeota, but its δ13C values still cannot be explained solely by autotrophic carbon fixation. Overall the complexity of the results suggests that both organic carbon assimilation (ca. 25% of total carbon) and multiple source(s) of exogenous GDGTs (contributing generally <30% of input to sediments) are necessary to explain the observed δ13CGDGT values. The results suggest caution when interpreting the total inputs of GDGTs to sedimentary records. Biogenic or open-slope sediments, rather than clastic basinal or shallow shelf sediments, are preferred locations for generating minimally-biased GDGT proxy records.

Introduction

Archaeal GDGTs are ubiquitous in marine sediments and form the basis of the sea surface temperature (SST) proxy known as TEX86 (Schouten et al., 2002). TEX86 has been used for paleoclimate reconstructions in both marine and large lacustrine environments, and over timescales from the Jurassic to the present (e.g., Bijl et al., 2010, Tierney et al., 2010, Jenkyns et al., 2012). The broad geographic and temporal range of GDGTs suggests they will continue to play an important role in interpreting paleotemperatures, even as the scientific community continues to study and debate the mechanistic control(s) on how TEX86 works (Elling et al., 2014, Elling et al., 2015, Qin et al., 2015). Although modern TEX86 calibrations generally predict SSTs to within ±3–5 °C (Liu et al., 2009, Kim et al., 2010, Tierney and Tingley, 2014), ancient records of TEX86-predicted SSTs can disagree with other proxies and climate models, particularly during greenhouse climates (e.g., Jenkyns et al., 2004, Hollis et al., 2012, Lopes dos Santos et al., 2013). Therefore it is critical to develop a better understanding of the mechanisms controlling GDGT production, export, and deposition (Pearson and Ingalls, 2013).

In most studies to date, the majority of archaeal GDGTs reaching marine sediments are believed to be sourced from planktonic, ammonia-oxidizing Thaumarchaeota, although there is some debate regarding possible additional sources (e.g., Lincoln et al., 2014). Cell numbers and maximum copies of archaeal ammonia monooxygenase (amoA) and 16S rRNA genes occur at or just below the base of the photic zone, coincident with nitrification (Massana et al., 1997, Karner et al., 2001, Francis et al., 2005, Church et al., 2010, Santoro et al., 2010). Lipid abundances follow patterns similar to gene copy numbers and cell counts (Schouten et al., 2012, Basse et al., 2014, Lincoln et al., 2014, Xie et al., 2014, Kim et al., 2016). Together these studies suggest that the majority of planktonic thaumarchaeal production is between 100 and 350 m, i.e., dominantly sub-photic. Sub-photic export of GDGTs is consistent with the ratio of GDGT-2 to GDGT-3 ([2/3]) observed in marine sediments. In suspended particulate matter (SPM), [2/3] increases as a function of water column depth, and sedimentary [2/3] values agree better with SPM below the photic zone (Turich et al., 2007, Taylor et al., 2013, Hernandez-Sanchez et al., 2014). Similarly, natural 14C data show that GDGTs recovered from sediments can have older “ages” than co-occurring phytoplanktonic lipids such as sterols (Pearson et al., 2001, Shah et al., 2008). Sub-photic water column export, however, cannot be easily distinguished from the confounding effects of erosional GDGT sources, or from inputs from benthic communities. Deep-water and sedimentary production, as well as exogenous inputs, both contribute “old” 14C, especially if the latter is due to the weathering of ancient sedimentary rocks.

Carbon assimilation in the ammonia-oxidizing Thaumarchaeota is believed to be dominantly, though not exclusively, autotrophic (Ouverney and Fuhrman, 2000, Könneke et al., 2005, Qin et al., 2014, Santoro et al., 2015). Although mixotrophy is observed in some strains, it apparently does not contribute the majority of lipid carbon (Wuchter et al., 2003), and the limited available evidence suggests the overall community assimilates ca. 80% of its lipid carbon directly from DIC (Ingalls et al., 2006). If these assessments are correct, the 13C content of GDGTs should generally reflect patterns of 13C in water column DIC. In support of this idea, δ13C values of archaeal biphytanes (C40 isoprenoid sidechains of GDGTs) are relatively constant across ocean basins and depositional environments, ca. −21‰ (c.f., Schouten et al., 2013). However, the assumption of a dominantly planktonic origin for sedimentary GDGTs has not been rigorously tested, and other studies indicate that non-planktonic sources of GDGTs may be important. In some sediments, biphytanes and GDGTs are observed with values ca. −25‰ (Smittenberg et al., 2005, Biddle et al., 2006), significantly outside the range of values observed for SPM (Hoefs et al., 1997). Although in these cases the anomalies were attributed to 13C–depletion within the local DIC pool or to in-situ heterotrophy mediated by Archaea growing within the sediments, alternative explanations are possible. These include mixotrophy or heterotrophy among planktonic Thaumarchaeota and contributions from heterotrophic Euryarchaeota (Iverson et al., 2012, Lincoln et al., 2014, Qin et al., 2014). More information is needed about how many sources and processes contribute GDGTs to sediments.

Conversely, if GDGTs in sediments are derived predominantly from autotrophic, planktonic export, they may serve as a paleo-δ13CDIC proxy (Hoefs et al., 1997, Schouten et al., 1998). Archaeal biphytanes have been used to infer the 13C content of dissolved inorganic carbon (DIC) during Cretaceous ocean anoxic events (Kuypers et al., 2001), previously a challenge due to the absence of carbonate sedimentation in many sections. This concept could be applied to other intervals of Earth history in which carbonates are absent or have been affected by diagenetic processes. Importantly, the use of δ13CGDGT values to reconstruct DIC is an idea that can be tested in the modern ocean. DIC is depleted in 13C in the Pacific Ocean relative to the Atlantic Ocean at depths below 100 m (Kroopnick, 1985). This represents an unexplored opportunity to validate the paleo-δ13CDIC proxy, as sub-photic growth of modern Thaumarchaeota would be expected to incorporate this inter-basinal signal.

To test this idea, we examined the 13C content of individual GDGTs extracted from five samples of Atlantic Ocean sediments and six samples of Pacific Ocean sediments to (i) test the idea that sedimentary δ13CGDGT values reflect local water-column profiles of δ13CDIC and (ii) evaluate whether exogenous and mixotrophic (or heterotrophic) inputs of GDGTs are likely to complicate these records. The choice of analytical approach is critical: inter-basinal differences in δ13CDIC are on the order of 1‰ and many geologic carbon isotope excursions of interest are <2‰ (e.g., ETM-2; Lourens et al., 2005). Here we use a novel method with analytical precision and accuracy ±0.25‰, a resolution that can distinguish minor differences between GDGT sources. Such a method opens a new window of opportunity to test the hypotheses described above.

Section snippets

Samples

Total lipid extracts (TLEs) were obtained from 12 horizons spanning 10 locations, all from archival samples (stored at −20 °C since collection or extraction; North Atlantic samples at −40 °C) (Table 1). The Santa Monica Basin (SMB) and Santa Barbara Basin (SBB) cores were described in Pearson et al. (2001) and Shah et al. (2008). The Cariaco Basin multicore was collected in 2004 and TLE was donated by K. Hughen. The Carolina Margin box core was collected off coastal North Carolina in July, 1996;

Precision and accuracy of δ13CGDGT measurements by SWiM-IRMS

The application of δ13CGDGT data to practical problems in (paleo)oceanography requires that the GDGT samples are sufficiently purified from background contamination, and that the isotope measurements are precise, accurate, and reproducible. We evaluated all of these factors systematically to develop quality control criteria.

Influence of autotrophy vs. mixotrophy on marine archaeal lipids

Planktonic Archaea, specifically the Group I.1a Thaumarchaeota (Delong, 1992, Fuhrman et al., 1992, Spang et al., 2010), account for most of the ocean’s ammonia oxidation (Francis et al., 2005, Könneke et al., 2005, Wuchter et al., 2006). To date, all pure and enrichment cultures of Thaumarchaeota (including the soil and hot springs Group I.1b (Pester et al., 2011), as well as marine taxa) are obligate carbon fixers, i.e., they oxidize ammonia for energy and they fix inorganic carbon (Könneke

Conclusions and future work

Modern marine sediments have variable δ13C values of GDGTs, both among individual GDGTs extracted from the same sediment, as well as among different locations on the same continental margin. The cause in both cases appears to be different fractional contributions from multiple sources, including – but not necessarily limited to – export of planktonic material from the water column and transport of weathered terrestrial sources (either soils or ancient sediments). The suite of samples studied

Acknowledgements

We thank Associate Editor Elizabeth Canuel and four anonymous reviewers for their valuable feedback. The following people provided access to samples and cruises: D. DeMaster (R/V Seward Johnson cruise, 1998; Carolina Margin sediment), K. Hughen and N. Drenzek (Cariaco; NSF OCE-0137005 and DEB-0447281), F. Prahl and S. Wakeham (Washington Margin sediments), Ellen Druffel (SMB/SBB sediments), and Tim Eglinton (N. Atlantic Line W cruise, 2010). Susan J. Carter provided laboratory assistance, and

References (102)

  • J. Hwang et al.

    Dynamics of particle export on the Northwest Atlantic margin

    Deep Sea Res. Part I

    (2009)
  • J.H. Kim et al.

    New indices and calibrations derived from the distribution of crenarchaeal isoprenoid tetraether lipids: implications for past sea surface temperature reconstructions

    Geochim. Cosmochim. Acta

    (2010)
  • J.-H. Kim et al.

    Biological source and provenance of deep-water derived isoprenoid tetraether lipids along the Portugese continental margin

    Geochim. Cosmochim. Acta

    (2016)
  • M. Könneke et al.

    Carbon isotope fractionation by the marine ammonia-oxidizing archaeon Nitrosopumilus maritimus

    Org. Geochem.

    (2012)
  • P.M. Kroopnick

    The distribution of C-13 of ∑-CO2 in the world oceans

    Deep Sea Res. Part A

    (1985)
  • E.A. Laws et al.

    Dependence of phytoplanktonic carbon isotopic composition on growth rate and CO2(aq) – Theoretical considerations and experimental results

    Geochim. Cosmochim. Acta

    (1995)
  • R.D. Pancost et al.

    Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation

    Geochim. Cosmochim. Acta

    (2001)
  • A. Pearson

    Lipidomics for geochemistry

  • A. Pearson et al.

    The origin of n-alkanes in Santa Monica Basin surface sediment: a model based on compound-specific Delta C-14 and delta C-13 data

    Org. Geochem.

    (2000)
  • A. Pearson et al.

    Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific Delta C-14 analysis

    Geochim. Cosmochim. Acta

    (2001)
  • M. Pester et al.

    The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology

    Curr. Opin. Microbiol.

    (2011)
  • F.G. Prahl et al.

    Terrestrial organic carbon contributions to sediments on the Washington Margin

    Geochim. Cosmochim. Acta

    (1994)
  • J.P. Saenz et al.

    Abundance and structural diversity of bacteriohopanepolyols in suspended particulate matter along a river to ocean transect

    Org. Geochem.

    (2011)
  • S. Schouten et al.

    Structural characterization, occurrence and fate of archaeal ether-bound acyclic and cyclic biphytanes and corresponding diols in sediments

    Org. Geochem.

    (1998)
  • S. Schouten et al.

    Evidence for anaerobic methane oxidation by archaea in euxinic waters of the Black Sea

    Org. Geochem.

    (2001)
  • S. Schouten et al.

    Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?

    Earth Planet. Sci. Lett.

    (2002)
  • S. Schouten et al.

    Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone: I. Selective preservation and degradation in the water column and consequences for the TEX86

    Geochim. Cosmochim. Acta

    (2012)
  • S. Schouten et al.

    The Org. Geochem. of glycerol dialkyl glycerol tetraether lipids: a review

    Org. Geochem.

    (2013)
  • F. Schubotz et al.

    Stable carbon isotopic compositions of intact polar lipids reveal complex carbon flow patterns among hydrocarbon degrading microbial communities at the Chapopote asphalt volcano

    Geochim. Cosmochim. Acta

    (2011)
  • S.R. Shah et al.

    Origins of archaeal tetraether lipids in sediments: insights from radiocarbon analysis

    Geochim. Cosmochim. Acta

    (2008)
  • R.H. Smittenberg et al.

    Pre- and post-industrial environmental changes as revealed by the biogeochemical sedimentary record of Drammensfjord, Norway

    Mar. Geol.

    (2005)
  • A. Spang et al.

    Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota

    Trends Microbiol.

    (2010)
  • A. Stadnitskaia et al.

    Application of lipid biomarkers to detect sources of organic matter in mud volcano deposits and post-eruptional methanotrophic processes in the Gulf of Cadiz, NE Atlantic

    Mar. Geol.

    (2008)
  • F.C. Tan et al.

    Organic carbon isotope ratios in recent sediments in the St. Lawrence estuary and the Gulf of St. Lawrence

    Estuarine Coastal Mar. Sci.

    (1979)
  • F.C. Tan et al.

    Sources, sinks and distribution of organic carbon in the St. Lawrence estuary, Canada

    Geochim. Cosmochim. Acta

    (1983)
  • K.W.R. Taylor et al.

    Re-evaluating modern and Palaeogene GDGT distributions: implications for SST reconstructions

    Global Planet. Change

    (2013)
  • C.J. Thomas et al.

    Organic carbon deposition on the North Carolina continental slope off Cape Hattaras (USA)

    Deep Sea Res. Part II

    (2002)
  • J.E. Tierney et al.

    A Bayesian, spatially-varying calibration model for the TEX86 proxy

    Geochim. Cosmochim. Acta

    (2014)
  • C. Turich et al.

    Lipids of marine Archaea: patterns and provenance in the water-column and sediments

    Geochim. Cosmochim. Acta

    (2007)
  • S.G. Wakeham et al.

    Archaea mediate anaerobic oxidation of methane in deep euxinic waters of the Black Sea

    Geochim. Cosmochim. Acta

    (2003)
  • J.J. Walsh et al.

    Organic storage of CO2 on the continental slope off the Mid-Atlantic Bight, the Southeastern Bering Sea, and the Peru Coast

    Deep Sea Res. Part II

    (1985)
  • C. Wuchter et al.

    Bicarbonate uptake by marine Crenarchaeota

    FEMS Microbiol. Lett.

    (2003)
  • J.E. Bauer et al.

    Isotopic constraints on carbon exchange between deep-ocean sediments and sea-water

    Nature

    (1995)
  • I.A. Berg et al.

    A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea

    Science

    (2007)
  • J.F. Biddle et al.

    Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru

    Proc. Natl. Acad. Sci. U.S.A.

    (2006)
  • P.K. Bijl et al.

    Transient middle Eocene atmospheric CO2 and temperature variations

    Science

    (2010)
  • M.J. Church et al.

    Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean

    Environ. Microbiol.

    (2010)
  • J.R. de la Torre et al.

    Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol

    Environ. Microbiol.

    (2008)
  • E.F. Delong

    Archaea in coastal marine environments

    Proc. Natl. Acad. Sci. U.S.A.

    (1992)
  • N.J. Drenzek

    The Temporal Dynamics of Terrestrial Organic Matter Transfer to the Oceans: Initial Assessment and Application

    (2007)
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    Present address: Institute of Geology & Mineralogy, University of Cologne, 50674 Cologne, Germany.

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