Elsevier

Geochimica et Cosmochimica Acta

Volume 261, 15 September 2019, Pages 383-395
Geochimica et Cosmochimica Acta

CO2-dependent carbon isotope fractionation in Archaea, Part II: The marine water column

https://doi.org/10.1016/j.gca.2019.06.043Get rights and content

Abstract

Stable carbon isotope ratios of archaeal glycerol dibiphytanyl glycerol tetraether (GDGT) lipids have been proposed as a proxy to infer past changes in the carbon isotope composition (δ13C) of dissolved inorganic carbon (DIC). The premise for paleo-δ13CDIC reconstructions from GDGTs is based on observations of relatively constant δ13CGDGT values in recent depositional environments. Marine Thaumarchaeota, thought to be the dominant source of GDGTs to marine sediments, fix inorganic carbon using the 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) pathway, which is specific to HCO3 as the substrate. Bicarbonate-dependent autotrophy has been the basis for predicting that the stable carbon isotopic composition of GDGTs (δ13CGDGT) should vary in parallel with water column δ13CDIC values, because HCO3 is by far the dominant fraction of DIC in modern seawater. However, this relationship has never been systematically tested. Here we examine the carbon isotopic composition of GDGTs from four water column profiles in the Southwest and Equatorial Atlantic Ocean. Values of δ13CGDGT increase with depth in the water column, in contrast to the characteristic decrease in δ13CDIC values. These divergent trends imply a decrease in the observed total biosynthetic isotope effect (εAr) with depth, i.e., the offset between δ13CDIC and δ13CGDGT is not constant. Instead, we find that values of εAr specifically correlate with oceanographic variables associated with extent of organic remineralization, decreasing as CO2 concentration increases. This observed relationship is consistent in both magnitude and direction with the results of an isotope flux-balance model for Thaumarchaeota that suggests εAr should be sensitive to growth rate (μ) and CO2 availability under conditions of atmospheric pCO2 < 4 times the pre-anthropogenic Holocene level. Further tests of the sensitivity of εAr to µ and CO2 in the modern marine environment will be essential to exploring the potential for a new, archaeal lipid-derived pCO2 paleobarometer.

Introduction

Glycerol dibiphytanyl glycerol tetraether (GDGT) lipids of archaeal membranes are preserved in marine sediments from the Jurassic to the present (e.g., Jenkyns et al., 2012). These biomarkers record the presence and activity of marine planktonic archaea, which are ubiquitous in the marine water column (Fuhrman et al., 1992, DeLong, 1992, Karner et al., 2001) and form the basis of the TEX86 paleotemperature proxy (Schouten et al., 2002).

The dominant source of GDGTs to sediments generally is believed to be the marine group I.1a Thaumarchaeota (e.g., Pearson and Ingalls, 2013). These archaea oxidize ammonia and fix carbon autotrophically using the 3–hydroxypropionate/4-hydroxybutyrate pathway (3HP/4HB) (Könneke et al., 2005, Berg et al., 2007, Könneke et al., 2014). Thaumarchaeota are most abundant and active near the base of the euphotic zone (Francis et al., 2005, Beman et al., 2008, Church et al., 2010, Santoro et al., 2010). Marine group II Euryarchaeota also are common, primarily in surface waters (Massana et al., 1997, Massana et al., 1998, Massana et al., 2000). Their presumed heterotrophic metabolism has largely been inferred from metagenomics due to a lack of cultured representatives (Frigaard et al., 2006, Iverson et al., 2012, Martin-Cuadrado et al., 2014, Orsi et al., 2015, Santoro et al., 2019). Recently Lincoln et al. (2014) proposed that these Euryarchaeota may also contribute to the GDGT pool, although this remains debated (Schouten et al., 2014), and to date only Thaumarchaeota are known to produce the distinctive cyclohexane ring-containing GDGT, crenarchaeol (Elling et al., 2017).

Due to the presumed dominance of total planktonic archaeal production by autotrophic Thaumarchaeota, stable carbon isotope measurements of GDGTs have been proposed as a tool to infer past changes in marine δ13CDIC values (Hoefs et al., 1997, Schouten et al., 1998), for example during Cretaceous ocean anoxic events (Kuypers et al., 2001) or other episodes where carbonate sedimentation is restricted or absent. However, the fidelity of a proposed paleo-δ13CDIC proxy requires that carbon assimilation by Thaumarchaeota be accompanied by a constant biosynthetic isotope effect (εAr, signifying the difference between the inorganic carbon source and the archaeal biomass), and that there be minimal influence from mixotrophic or heterotrophic carbon assimilation, including any contributions by Euryarchaeota.

To date, preliminary evidence that GDGTs could serve as a paleo-δ13CDIC proxy has invoked the relatively constant δ13C value of −21 ± 1.5‰ for the crenarchaeol-specific C40:3 biphytane (sidechain hydrocarbon) observed in recent depositional environments (Schouten et al., 2013). The 3HP/4HB pathway of carbon fixation in Thaumarchaeota is specific to HCO3, leading to the supposition that a relatively stable ocean δ13CDIC signature (mostly reflecting δ13CHCO3− values), high and relatively invariant [HCO3], and a constant biosynthetic εAr value would lead to stable values of δ13CGDGT for the entire exported pool of water-column GDGTs.

However, a limited survey of recent core-top sediments showed that δ13CGDGT values, including the Thaumarchaeota-specific crenarchaeol, are not truly constant with respect to δ13CDIC values (Pearson et al., 2016). This finding, plus earlier carbon isotopic measurements (Ingalls et al., 2006), were interpreted as reflecting a small but significant (~20%) contribution of heterotrophically-assimilated organic carbon by the total archaeal community. Although marine Thaumarchaeota take up amino acids (Ouverney and Fuhrman, 2000, Teira et al., 2004, Herndl et al., 2005, Qin et al., 2014), and some strains of soil-group I.1b Thaumarchaeota appear to require pyruvate supplementation (Tourna et al., 2011), recent work has proposed that the role for organic acids is to detoxify oxygen radicals formed as a byproduct of ammonia oxidation (Kim et al., 2016). Organic carbon does not appear to be incorporated into biomass, nor do organic substrates actually promote growth (Kim et al., 2016). This would suggest that lipid isotope studies may have overestimated the contribution of mixotrophy or heterotrophy to Thaumarchaeota, and that other factors should be considered in the interpretation of non-constant δ13CGDGT values.

Here we investigated the 13C content of individual GDGTs previously quantified (Hurley et al., 2018) from a water-column transect in the Southwest and Equatorial Atlantic Ocean (∼40°S to 10°N). Our results show that δ13CGDGT values vary inversely to the gradient of δ13CDIC, and that εAr differs both between locations and with depth. These patterns are not correlated with δ13C values for particulate organic carbon (δ13CPOC) and are not well explained by heterotrophic processes. Instead, the response of εAr is consistent with a recent model that suggests δ13CGDGT values for Thaumarchaeota should respond to in situ pH and [CO2(aq)] (Pearson et al., 2019). Although the magnitude of the CO2-dependence is small, showing a total range of < 5‰ for εAr through the water column, the consistency between the data and the model suggest that δ13CGDGT values – specifically those measured for crenarchaeol – could be used as a pCO2 proxy. Previously-reported δ13CGDGT values from sediments are reinterpreted within this framework and highlight both the promise and limitations of the application.

Section snippets

Methods

Our sampling and extraction approach is described in detail in Hurley et al. (2018). Briefly, samples were collected from aboard the R/V Knorr during the “DeepDOM” cruise, KN210-04, in March–May 2013 from 38.0°S 45.0°W (Station 2), 22.5°S 33.0°W (Station 7), 2.7°S 28.5°W (Station 15) and 9.7°N 55.3°W (Station 23) (Fig. 1). The deep chlorophyll maximum was found at 70 m (Station 23), 60–70 m (Station 15), 125 m (Station 7), and 50–75 m (Station 2) (Hurley et al., 2018). Suspended particulate

Results

The DeepDOM cruise track (Fig. 1) traversed the equatorial and subtropical gyre surface regimes and deep water masses of North Atlantic Deep Water (NADW) and Antarctic Intermediate Water (AAIW). We analyzed samples from four stations: Station 23 at the edge of the Amazon River plume, Station 15 in the productive equatorial region, Station 7 in the South Atlantic gyre and Station 2 in the southern subtropical transition zone. Values of δ13C for bulk particulate organic carbon (POC) in the

Metabolic and ecological inferences

This study presents the first comprehensive water column profiles of δ13CGDGT values, providing unique insights into the metabolic function and physiology of Thaumarchaeota. The offsets between the δ13CGDGT values and the potential carbon sources for Thaumarchaeota are consistent with predominantly autotrophic carbon fixation, the isotope effect of which is dependent on CO2 concentration. When interpreted in the context of CO2– and growth rate-dependent εAr, the data also suggest that despite

Conclusions

An isotope flux-balance model based on kinetic modeling of 3HP/4HB pathway physiology (Part I companion paper; Pearson et al., 2019) suggests that carbon isotope fractionation (εAr) in marine Thaumarchaeota should be sensitive to growth rate (μ) and CO2 availability under conditions of atmospheric pCO2 < 4 times the pre-anthropogenic Holocene level. Here we showed that values of δ13CGDGT from four water column profiles in the Southwest and Equatorial Atlantic Ocean support the premise of that

Acknowledgments

We thank Boswell Wing, Sebastian Kopf, David Johnston, and Eric Ellison for valuable discussions. We thank Joe Werne for editorial assistance and three anonymous reviewers for valuable comments. We are grateful to the crew, chief scientists E. Kujawinski and K. Longnecker, and the scientific shipboard part of R/V Knorr cruise KN201-04. Funding for the cruise was provided by the National Science Foundation (NSF-1154320 to E. Kujawinski and K. Longnecker, WHOI). AP, SJH, and FE acknowledge

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