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Fluid Mixing and the Deep Biosphere of a Fossil Lost City-Type Hydrothermal System at the Iberia Margin

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Fluid Mixing and the Deep Biosphere of a Fossil Lost City-Type Hydrothermal System at the Iberia Margin Fluid mixing and the deep biosphere of a fossil Lost City-type hydrothermal system at the Iberia Margin Frieder Kleina,1, Susan E. Humphrisb, Weifu Guob, Florence Schubotzc, Esther M. Schwarzenbachd, and William D. Orsia aDepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; bDepartment of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA 02543; cDepartment of Geosciences and Center for Marine Environmental Sciences, University of Bremen, 28334 Bremen, Germany; and dDepartment of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved August 4, 2015 (received for review March 7, 2015) Subseafloor mixing of reduced hydrothermal fluids with seawater is aging, brucite undersaturated in seawater dissolves and aragonite believed to provide the energy and substrates needed to support recrystallizes to calcite (7). deep chemolithoautotrophic life in the hydrated oceanic mantle (i.e., Actively venting chimneys host a microbial community with a serpentinite). However, geosphere-biosphere interactions in serpen- relatively high proportion of methanogenic archaea (the Lost tinite-hosted subseafloor mixing zones remain poorly constrained. City Methanosarcinales), methanotrophic bacteria, and sulfur- Here we examine fossil microbial communities and fluid mixing oxidizing bacteria, whereas typical sulfate-reducing bacteria are processes in the subseafloor of a Cretaceous Lost City-type hydro- rare (8–10). Geochemical evidence for significant microbial sulfate thermal system at the magma-poor passive Iberia Margin (Ocean reduction in basement lithologies and distinct microbial commu- Drilling Program Leg 149, Hole 897D). Brucite−calcite mineral assem- nities in Lost City vent fluids and chimneys suggest that subsurface blages precipitated from mixed fluids ca. 65 m below the Cretaceous communities may be different from those in chimney walls (8, 9, ± 3 paleo-seafloor at temperatures of 31.7 4.3 °C within steep chemical 11). The lack of modern seawater bicarbonate and low CO2/ He in gradients between weathered, carbonate-rich serpentinite breccia Lost City fluids clearly indicate bicarbonate removal before vent- and serpentinite. Mixing of oxidized seawater and strongly reducing ing, but it remains unclear if bicarbonate removal occurred by hydrothermal fluid at moderate temperatures created conditions “dark” microbial carbon fixation in a serpentinization-fueled capable of supporting microbial activity. Dense microbial colonies deep biosphere, by carbonate precipitation, or both (12). are fossilized in brucite−calcite veins that are strongly enriched in Other active and fossil seafloor hydrothermal systems similar organic carbon (up to 0.5 wt.% of the total carbon) but depleted in to Lost City exist in a range of seafloor environments, including 13 δ13 = − ‰ C( CTOC 19.4 ). We detected a combination of bacterial di- the Mid-Atlantic Ridge (13), New Caledonia (14), and the Mariana ether lipid biomarkers, archaeol, and archaeal tetraethers analogous forearc (15, 16). Bathymodiolus mussels are, in some places, as- to those found in carbonate chimneys at the active Lost City hydro- sociated with these systems, suggesting that active serpentiniza- thermal field. The exposure of mantle rocks to seawater during the tion is supporting not only microbial chemosynthetic ecosystems breakup of Pangaea fueled chemolithoautotrophic microbial commu- but also macrofaunal communities (16). However, biological nities at the Iberia Margin, possibly before the onset of seafloor processes in the subseafloor of these Lost City-type systems are spreading. Lost City-type serpentinization systems have been discov- poorly understood. ered at midocean ridges, in forearc settings of subduction zones, and at continental margins. It appears that, wherever they occur, they can Serpentinization at Magma-Poor Continental Margins support microbial life, even in deep subseafloor environments. The breakup of (super)continents exposes large volumes, on the order of thousands of cubic kilometers (17), of mantle peridotite serpentinization | microfossils | lipid biomarkers | brucite−calcite | passive margin to seawater, making magma-poor continental margins a prime erpentinized mantle rocks constitute a major component of Significance Soceanic plates, subduction zones, and passive margins. Serpen- tinization systems have existed throughout most of Earth’shistory, We provide biogeochemical, micropaleontological, and petro- and it has been suggested that mixing of serpentinization fluids with logical constraints on a subseafloor habitat at the passive Iberia Archean seawater produced conditions conducive to abiotic syn- Margin, where mixing of reduced hydrothermal serpentiniza- thesis and the emergence of life on Earth (1). The Lost City hy- tion fluids with oxic seawater provided the energy and sub- drothermal field, located ∼15 km off the Mid-Atlantic Ridge axis at strates for metabolic reactions. This mixing zone was inhabited 30°N (2–4), represents the archetype of low-temperature seafloor by bacteria and archaea and is comparable to the active Lost serpentinization systems at slow-spreading midocean ridges and City hydrothermal field at the Mid-Atlantic Ridge. Our results serves as an excellent present-day analog to fossil serpentinite- highlight the potential of magma-poor passive margins to host hosted hydrothermal systems in such environments. Lost City vents Lost City-type hydrothermal systems that support microbial warm (≤ 91 °C), high-pH (9–11) fluids enriched in dissolved cal- activity in subseafloor environments. Because equivalent sys- cium, H2,CH4, formate, and other short-chain hydrocarbons (2, 5, tems have likely existed throughout most of Earth’s history in a 6). In contrast to high-temperature black smoker-type chimneys wide range of oceanic environments, fluid mixing may have consisting of Cu−Fe sulfides, the Lost City chimneys are composed provided the substrates and energy to support a unique sub- of brucite and calcium carbonate (aragonite, calcite), which form seafloor community of microorganisms over geological timescales. when serpentinization fluids (SF) mix with seawater (SW) (7), Author contributions: F.K. designed research; F.K., W.G., F.S., and E.M.S. performed re- + À À 2 + + = + search; F.K., W.G., F.S., and E.M.S. contributed new reagents/analytic tools; F.K., S.E.H., Ca OH HCO3 CaCO3 H2O SF SF SW W.G., F.S., E.M.S., and W.D.O. analyzed data; and F.K., S.E.H., W.G., F.S., E.M.S., and W.D.O. wrote the paper. 2+ + À = ð Þ The authors declare no conflict of interest. Mg 2OH Mg OH 2. SW SF This article is a PNAS Direct Submission. 1To whom correspondence should be addressed. Email: [email protected]. Nascent Lost City chimneys are dominated by aragonite and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. brucite, whereas older structures are dominated by calcite. During 1073/pnas.1504674112/-/DCSupplemental. 12036–12041 | PNAS | September 29, 2015 | vol. 112 | no. 39 www.pnas.org/cgi/doi/10.1073/pnas.1504674112 Downloaded by guest on September 23, 2021 in most recovered samples and produced serpentine (lizardite + 3000 2000 5000 4000 chrysotile), brucite, minor chlorite, and traces of magnetite and Iberia 2000 other opaque minerals. Thermodynamic constraints and hydro- 637 639 641 1000 thermal experiments suggest that serpentinization fluids associ- ated with this assemblage are alkaline, depleted in dissolved 640 638 − 2− inorganic carbon (ΣCO2 = CO2, HCO3 ,CO3 ), SiO2, and Mg Iberia Abyssal Plain but enriched in dissolved Ca and H2 compared with seawater 3000 Vigo (30, 31). Accessory opaque minerals include valleriite, pent- 897 landite, millerite, chalcopyrite, siegenite, polydymite, and pyrite, 899 − 1069 398 in addition to the relict Ni Fe alloy awaruite and native Cu (26). 1065 1070898 Awaruite, armored by magnetite from dissolution, indicates 900 9014000 Serpentinized basement strongly reducing conditions and low sulfur fugacities during the 1067-68 Continental crust main stages of active serpentinization (26). Later, conditions Basement not reached became less reducing and sulfur fugacities increased, as indicated Drilled continental basement 100 km 5000 Drilled serpentinite basement by sulfur-rich sulfides such as millerite and polydymite. Opaque minerals in ophicalcite, including pyrite, millerite (26), hematite, Fig. 1. Simplified geological map of the Iberia Margin showing the locali- and goethite, record oxidizing conditions due to prolonged in- ties of drill sites from Ocean Drilling Program Legs 103, 149, and 173. Sam- gress of cold, oxidized seawater, which also led to precipitation of ples analyzed in this study are from Site 897. Interpretation of geological clay minerals and quartz at the expense of serpentine at temper- units is based on drilling results and geophysical surveys (drill site locations ≤ and geological interpretation from ref. 60). atures 100 °C (32). The mineralogical differences between the upper ophicalcite section and the deeper serpentinite section provide evidence for strong chemical gradients in pH, fO2, ΣCO2, 2− target area to search for Lost City-type hydrothermal activ- and SO4 over a short interval between ∼60 m and 70 m below ity. The archetypal example of magma-poor rifted margins, the the sediment−basement interface. Iberia Margin, has been examined by seafloor drilling and
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