Sub-seafloor sulfur cycling in a low-temperature barite field: A multi-proxy study from the Arctic Loki’s Castle vent field

Abstract

The Loki's Castle vent field at the ultraslow-spreading Arctic Mid-Ocean Ridge (AMOR) hosts a low-temperature venting area, which is characterized by microbial mats and numerous up to 1 m tall barite chimneys. An actively-venting barite chimney yielded δ¹⁸O_SO4 and δ³⁴S_SO4 values heavier than ambient seawater and sulfide-oxidizing bacteria in microbial mats identified microbial sulfate reduction and sulfide oxidation as the main processes. In order to investigate the chemical and microbial structure below the barite field, we obtained two gravity cores and present chemical composition (e.g., H₂S, SO₄²⁻, NH₄⁺, DIC) and stable isotope data for the pore fluids (δ³⁴S_SO4, δ¹³CDIC) together with stable isotope (δ¹³C_org, δ³⁴S, ∆³³S) and lipid biomarker data on bulk sediments. The gravity core more distant to the high-temperature vents shows seawater-like pore fluid profiles with only minor vent fluid contribution (<1%), whereas the bulk sediments yield negative δ³⁴S and positive ∆³³S values indicative of sulfate reduction. In contrast, the pore fluid data in close proximity to the high-temperature vents (5–9% vent fluid contribution) record distinct horizons showing sulfate depletion, which coincide with δ³⁴S_SO4 values that are higher than those for ambient seawater sulfate. The sediments in these horizons record negative δ³⁴S and positive ∆³³S values, indicating that both the pore fluids and the sediments are influenced by active sulfate reduction. We also detected a greater abundance of archaeal mono- and dialkyl tetraether lipids (GMGTs, GDGTs) and bacterial fatty acids in the sediments at actively venting sites, pointing to a more diverse microbial community. Moreover, a positive correlation observed between GMGT abundance and sulfur concentration in the sediments indicates that the availability of sulfur is crucial for the presence of GMGT-producing archaea. Our multi-proxy approach suggests that sulfate reduction in the sub-seafloor sediments of the Loki's Castle barite field is largely driven by microbial processes.

Introduction

Hydrothermal activity in deep-sea hydrothermal systems at mid-ocean ridges is driven by the heating of seawater percolating through the ocean crust by a magmatic heat source and results in the discharge of reduced high-temperature vent fluids (e.g. Schultz and Elderfield, 1997). This interaction causes steep temperature and chemical gradients, which creates microhabitats for thermophilic microbial communities and provides metabolic energy for chemolithoautotrophy (Tivey, 1995; McCollom and Shock, 1997; Miroshnichenko, 2004). The formation of black smoker chimneys and associated mineral deposits is well characterized, but the geobiological processes in related sub-seafloor sediments influenced by diffuse venting of low-temperature fluids are less well understood (e.g. Nunoura et al., 2010). The lower temperatures in sub-seafloor sediments result from the higher admixture of seawater, making them promising target sites for active and diverse microbial communities (Amend and Teske, 2005; Amend et al., 2011). Thermodynamic and numerical calculations identify sulfide oxidation as the predominant energy source over a wide range of temperatures in basalt-hosted hydrothermal systems (Amend et al., 2011).

Sulfur is a key element in hydrothermal systems, making its sulfur isotopic composition a powerful tool to investigate the sulfur cycling between different habitats and to distinguish biological and non-biological processes (Ono et al., 2007, Ono et al., 2012; Peters et al., 2010, Peters et al., 2011; Aoyama et al., 2014; Eickmann et al., 2014; Jaeschke et al., 2014; McDermott et al., 2015). The main processes controlling the sulfur isotopic composition of hydrogen sulfide in hydrothermal fluids and therefore of sulfides in hydrothermal sediments are isotope exchange reactions between dissolved sulfate and sulfide, as well as biological fractionation processes. Thus, combining δ³⁴S and ∆³³S values allow identifying different mass-dependent fractionation processes, even if δ³⁴S values are identical. It has been experimentally shown, for instance, that sulfate-reducing bacteria produce hydrogen sulfide with negative δ³⁴S and slightly positive ∆³³S values (Johnston et al., 2007). Microbial sulfate reduction has been identified as a key microbial process during the low-temperature alteration of oceanic crustal rocks (Rouxel et al., 2004; Ono et al., 2012). Studies of fluids circulating through oceanic basement rocks on the eastern flank of the Juan de Fuca Ridge, or through active hydrothermal systems (Tyrrhenian Sea, Okinawa Trough), corroborate this finding and identify the presence of sulfate-reducing microorganisms at considerable depths in these settings (Rudnicki et al., 2001; Peters et al., 2011; Aoyama et al., 2014). There are, however, only a few studies that were able to obtain sediment cores from active hydrothermal systems.

Another way to investigate the complex microbial community structures in hydrothermal systems are culture-independent molecular approaches based on 16S rRNA gene analysis, as well as enrichment and isolation studies (Takai et al., 2001; Schrenk et al., 2003; Kormas et al., 2006; Jaeschke et al., 2012). These studies revealed a remarkable microbial diversity of typical (hyper)thermophilic archaea predominant in the high temperature zones of the chimney interiors, while mesophilic to moderately thermophilic bacteria and Marine group I (MGI) Thaumarchaeota dominate diffuse flow-specific communities and chimney wall surfaces (Kato et al., 2010; Jaeschke et al., 2012; Campbell et al., 2013; Dahle et al., 2015; Steen et al., 2016). Organic geochemistry can provide a complementary view on both active and fossil microbial communities by means of lipid biomarker analysis (Blumenberg et al., 2012; Méhay et al., 2013; Jaeschke et al., 2012, Jaeschke et al., 2014; Pan et al., 2016; Li et al., 2018). Archaea possess unique membranes predominantly composed of diether lipids (archaeol) or glycerol mono and dialkyl glycerol tetraether lipids (GMGT and GDGT). Specific structural adaptations (i.e. cyclization) are believed to make the archaeal membrane more suitable for life in extreme environments than the ester-type bilayer lipids of bacteria (Van de Vossenberg et al., 1998). The introduction of an additional covalent cross-link between the isoprenoid chains in GMGTs is thought to help maintain membrane stability at high temperatures (Morii et al., 1998; Sugai et al., 2004). GMGTs are as yet detected in several groups of (hyper)thermophilic Euryarchaeota and Crenarchaeota (Sugai et al., 2004; Schouten et al., 2008b; Knappy et al., 2011). Indeed, detection of abundant GMGTs with 1–4 cyclopentane rings in natural environments have so far been restricted to the interior hot parts of black smoker walls (Jaeschke et al., 2012; Li et al., 2018) and terrestrial hot springs (Jia et al., 2014). However, their function in archaeal physiology is still not well understood. Besides thermal stress, other parameters could also be controlling the lipid composition in archaea such as pH, pressure, heavy metal content or a specific metabolism (Uda et al., 2004; Boyd et al., 2011; Jia et al., 2014).

Microbial and lipid biomarker studies identified sulfide-oxidizing bacteria on the outer surfaces of black smokers and in microbial mats from the Loki's Castle vent field, a basalt-hosted hydrothermal system at the Arctic Mid-Ocean Ridge (AMOR; Jaeschke et al., 2012; Steen et al., 2016). High methane (CH₄) and ammonium (NH₄⁺) concentrations in the high-temperature vent fluids suggested the existence of buried sediments underneath the volcanic ridge (Pedersen et al., 2010; Baumberger et al., 2016b). Consequently, the interaction of ascending high-temperature fluids and buried sediments may provide additional energy sources besides sulfur oxidation for chemolithoautotrophic microorganisms, e.g., through ammonium and methane oxidation. Here we present a combination of chemical composition, stable isotope and lipid biomarker data along two gravity cores from a low-temperature barite field at Loki's Castle to provide first comprehensive insights into sub-seafloor processes. We further present a mixing model based on pore fluid chemistry and the first combination of multiple sulfur isotope and lipid biomarker data to investigate the potential role of microbial sulfate reduction in sub-seafloor hydrothermal sediments.