The role of prokaryotes in supergene alteration of submarine hydrothermal sulfides

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Abstract

We combine mineralogical, stable isotope and organic biomarker data to understand the role of prokaryote activity in supergene reactions within submarine hydrothermal sulfidic sediments. Data are presented for two adjacent cores from the periphery of the inactive Alvin hydrothermal mound. The limit of oxygenated seawater penetration into the sulfidic sediments is expressed as a sharp peak in solid phase Cu (atacamite and secondary Cu sulfides) associated with supergene alteration of the sulfide pile. Total prokaryote numbers are low throughout the upper few metres of sediment relative to published data for deep-sea sites. However, there is a statistically significant enrichment of prokaryote numbers at the redox front that coincides with abundant Fe-oxide filaments and a unique distribution of microbial biomarkers. The dominance of quaternary-branched alkanes in the oxidized transition zone immediately above the redox front (and their absence below) suggests a significant role of the source organisms in iron or sulfide oxidation under the more circumneutral conditions associated with the redox transition zone. The morphology of the Fe-oxide filaments preserved within late stage silica and gypsum mineralization is consistent with a biogenic origin of the filaments. Gypsum sulfur isotopes are in equilibrium with fluids that are derived from quantitative sulfide oxidation and gypsum nucleation is inferred to be biologically induced. These new data suggest that supergene alteration of sulfidic sediments generates sharp redox and pH gradients that stimulate prokaryotic activity, in particular iron and sulfide oxidisers, which in turn govern the distribution of secondary mineral phases and the abundance of redox sensitive trace metals.

Introduction

Large numbers of prokaryote cells have been enumerated in a variety of sedimentary settings to depths of up to 800 m below the seafloor (e.g., [1]). Approximately 10–30% of the cells are viable and metabolically active, even at several 100 m depth [2]. Some of the lowest cell counts observed in the upper few metres of deep-sea sediments come from metalliferous sediments associated with mid-ocean ridge hydrothermal systems [3] and eastern equatorial Pacific open ocean sites [4]. The low cell abundance, coupled to very low levels of reaction products in pore fluids, have been taken to imply low net metabolic reaction rates in these sediments [3], [4]. Alternative analytical approaches (including polymerase chain reaction amplification of 16S rRNA) in similar settings have demonstrated a wide diversity of active bacterial and archaeal assemblages in hydrothermal sediments [5]. Cell counts and measurements of metabolites may not, therefore, yield a complete record of prokaryotic reaction rates and metabolic turnover [6], [7]. Hence, our current understanding of the activity of specialised hydrothermal sediment prokaryotic communities remains limited.

Fe-oxides and oxyhydroxides are the major oxidised component of hydrothermal deposits at seafloor vent sites [8]. Sulfide alteration within submarine metalliferous sediments has been compared with subaerial supergene processes [9], [10], where in addition to inorganic oxidation processes, morphological evidence suggests that microbial activity plays a significant role in the formation of hydrothermal Fe-oxide deposits [11]. This hypothesis is supported by compelling evidence from in situ incubations combined with 16S rRNA, fluorescent in situ hybridisation (FISH) and cultures of Fe-oxidising bacteria from a variety of hydrothermal settings [12], [13], [14], [15]. Microbial activity dominates Fe2+ oxidation under low pH conditions where inorganic oxidation is kinetically limited (e.g., subaerial acid mine drainage) and may also play an important role in the formation of hydrothermal Fe-oxide deposits under circumneutral pH conditions [12], [13], [14]. However, it has proved difficult to determine the function and impact of specific prokaryotic activity in the wide range of natural hydrothermal settings.

Sediments surrounding hydrothermal mounds contain collapsed sulfide chimney material juxtaposed with oxic substrates [16], creating sharp chemical and physical gradients that generate a range of habitats suitable for prokaryote exploitation. We hypothesise that maximum prokaryotic activity occurs in localised redox zones associated with in situ sulfide alteration. Rapid turnover of redox sensitive species within these micro-zones limits the impact on pore fluid chemistry and cell counts, but may play a significant role in the fate of hydrothermal deposits on the seafloor. This study combines mineralogical and stable isotope investigation with lipid biomarker analyses, with the aim of studying the impact of prokaryotic metabolism on the mineralogy and geochemistry of hydrothermal sediment undergoing seafloor alteration.

Section snippets

Geological setting and Alvin zone sediments

The Alvin zone is a discontinuous, elongate group of inactive sulfide mounds ∼ 2 km long (NE–SW) by 1 km wide (NW–SE) and is located 2–4 km NNE of the active TAG mound at water depths of 3400–3600 m on the Mid-Atlantic Ridge [17] (Fig. 1). The sediment cores studied here were taken from the southernmost of these mounds (the Alvin mound). This mound is ∼ 200 m in diameter and 28 m high, and is similar in size to the nearby active TAG mound [18]. However, heat flow and temperature across the mound are

Sampling and methodology

Two ∼ 2 m gravity cores: CD102/43 and CD102/58 (26°09.26′N, 44°48.90′W), were collected from the southern periphery of the Alvin mound during cruise CD102 of the RV Charles Darwin [26]. A background pelagic core (CD102/10) was also retrieved for direct comparison of deep-sea microbial abundances [3]. Coring was carried out within a 4-receiver transponder net, with a further transponder mounted 25 m above the corer. Navigation records indicate that core 58 was taken ∼ 35 m due north of core 43 [26].

Results

The stratigraphy and geochemistry of core 43 have been described in detail [3], [20] and are broadly similar to core 58. Both cores contain a surface layer of pelagic carbonate that varies in thickness across the Alvin zone as sediments are redistributed in the rough topography of the median valley [16]. The significant post depositional sediment redistribution and carbonate dissolution preclude any precise estimates of stratigraphic age within these cores.

Below the carbonate cap (52 cmbsf in

Discussion

Oxygen penetration into Cu-bearing hydrothermal sediments leads to oxidation of pyrite and chalcopyrite, a decrease in pH and Cu mobilisation and re-precipitation at the supergene reaction front (Fig. 2, Fig. 3; [35]). This generates a peak in solid phase Cu (as a combination of atacamite and secondary Cu-sulfides) that can be used to track the penetration of oxygen into the sediment (Fig. 3a–f). The depth interval above the supergene reaction front, between the Mn and Cu solid phase peaks,

Conclusions and wider implications

There is a specialized prokaryote community present in hydrothermal sediments with low total cell numbers, although a significant stimulation of activity (doubling of cell counts) is associated with active redox fronts [3]. This stimulation is manifest as unusual quaternary-branched hydrocarbon biomarkers and dense Fe-oxide filament occurrences associated with supergene alteration products in the shallow subsurface of the hydrothermal mound. These filaments served, in turn, as nuclei for

Acknowledgements

We are grateful to captain and crew of RRS Charles Darwin for their assistance during the BRIDGE Cruise CD 102. Particular thanks to B. Cragg and J. Parkes for useful discussions, and M. Rudnicki and J. Rhodes for help with shipboard and other analyses. R. Jones, J. Ford and R. Pearce are thanked for help with sample preparation. We also thank B. van Dongen for performing organic geochemical analyses, and I. Bull and R. Berstan for technical support. This research was funded by the Natural

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