Stable carbon isotope ratios of intact GDGTs indicate heterogeneous sources to marine sediments
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
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Present address: Institute of Geology & Mineralogy, University of Cologne, 50674 Cologne, Germany.