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Marine dissolved organic carbon (DOC) is highly depleted in radiocarbon and thus inferred to be largely refractory to removal processes that operate on less than millennial timescales. However, a growing number of reports have shown that a large fraction of marine DOC can be effectively removed during circulation through submarine hydrothermal systems. What is not clear, however, is whether the DOC that remains in hydrothermal fluids is remnant non-reactive DOC from recharged seawater, or DOC that has been largely produced in the subsurface. We collected and characterized warm (∼65 °C) hydrothermal fluids from deep (18, 40, 73, 200 m) within the basalt-hosted basement of the Juan de Fuca Ridge flank in the Northeast Pacific Ocean. DOC concentrations in hydrothermal fluids were 9 to 18 μM, much lower than measured in local deep seawater (37.5 μM). DOC Δ 14 C values of −683‰ to −856‰ were much lower than the Δ 14 C-dissolved inorganic carbon (DIC) values of −880‰ to −918‰, while DOC δ 13 C values of −23.6‰ to −27.0‰ were much heavier than that of the particulate organic carbon (POC) pool ( ∼ − 34 ‰ ), suggesting that biological production in the subsurface is not a primary source of DOC. Rather, our data suggest that isotopically enriched DOC are selectively removed from recharged seawater, leaving DOC that is very isotopically depleted in the basaltic basement fluids. Despite the removal of 50–75% of DOC in the subsurface, nuclear magnetic resonance (NMR) functional group analyses indicate that aromatic compounds were added to basaltic basement fluids during passage through the deep subseafloor and may partly contribute to the depleted 14C DOC in the ridge-flank basement fluids.

With large topographic gradients, rifted basins serve as efficient traps for particulate matter from adjacent lands and the ocean surface. However, the fate of organic carbon in the sediment, mostly unaltered by the hydrothermal activities known to occur in young rifts, remains poorly understood. In this study, we present an examination of diagenetic activities and carbon remineralization based on the first complete suite of pore-water data of sediment marginally affected by hydrothermal activities in the Southern Okinawa Trough (SOT). The sediment showed an oxygen penetration depth of 1 cm, consumption of NO3- in the top 1 cm, smeared profiles of Mn2+ and Fe2+ with the latter reaching up to 450 μmol L-1, and relatively unchanged SO42- concentrations with depth. Net production rates of dissolved species resolved from pore-water profiles provide an estimate of 1.68 ± 0.21 mmol C m-2 d-1 as the total carbon remineralization rate in the upper 30 cm sediment column, with aerobic carbon oxidation being the major pathway. The rate, one order of magnitude lower than that of the adjacent East China Sea, is attributed to the lower bottom-water temperature and carbon flux in the trough. The high carbon burial efficiency of SOT (68% of carbon reaching the seafloor and processed thereunder) reflects the combined effects of small mountain rivers and rifting-induced particle trapping.

The degassing of primordial gases from Earth's interior is evidenced by the high He 3 / 4 He ratios in submarine hydrothermal plumes, vent fluids, and rock samples with mantle origin from active hydrothermal systems in mid-ocean ridges (MOR) and subduction zone volcanism. As the largest aquifer on Earth, the uppermost 40-500 m of permeable submarine ridge flank basement (1-65 million-years-old, Myr) holds ∼2% of the ocean volume and accounts for 70% of the seafloor hydrothermal heat flux. However, the degassing of primordial gases through the oceanic ridge flank crust has not yet been directly quantified. Here, we show that high integrity hydrothermal (65 °C) fluids from the sediment-buried 3.5 Myr basaltic crust from the eastern flank of the Juan de Fuca Ridge (JdFR) contain elevated 3He. The He 3 / 4 He for the basaltic fluid is 4.5 ± 0.1 R a (relative to the air ratio), which is greatly elevated when compared to deep seawater (1.05 R a ), but is half of that observed for high-temperature vent fluids (∼8 R a ) emitting from MOR. Only a small fraction of the 3He in ridge flank fluids is derived from the entrainment of high-temperature ridge-axis fluids and is better explained by degassing of the mantle through the mantle-crust boundary. The lower than MOR He 3 / 4 He ratios indicate that radiogenic 4He originates from aged uranium and thorium decay within the mantle as well as from the ridge-flank basalts. The 3He outgassing through warm ridge flanks (4.9 to 36 mol/yr) accounts for 0.7-6% of the global 3He outgassing, exceeded only by degassing through mid-ocean ridges and subduction volcanism. The presence of mantle 3He suggests that the abiogenic methane present in the ridge flank fluids might be mantle-derived. Based on the 3He outgassing flux, a possibly mantle-derived abiotic methane production rate at the ridge flank is estimated to be 0.3 – 35 × 10 8 mol / yr .

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The oceanic basaltic basement contains the largest aquifer on Earth and potentially plays an important role in the global carbon cycle as a net sink for dissolved organic carbon (DOC). However, few details of the organic matter cycling in the subsurface are known because great water depths and thick sediments typically hinder direct access to this environment. In an effort to examine the role of water–rock–microorganism interaction on organic matter cycling in the oceanic basaltic crust, basement fluid samples collected from three borehole observatories installed on the eastern flank of the Juan de Fuca Ridge were analyzed for dissolved amino acids. Our data show that dissolved free amino acids (1–13 nM) and dissolved hydrolyzable amino acids (43–89 nM) are present in the basement. The amino acid concentrations in the ridge-flank basement fluids are at the low end of all submarine hydrothermal fluids reported in the literature and are similar to those in deep seawater. Amino acids in recharging deep seawater, in situ amino acid production, and diffusional input from overlying sediments are potential sources of amino acids in the basement fluids. Thermodynamic modeling shows that amino acid synthesis in the basement can be sustained by energy supplied from inorganic substrates via chemolithotrophic metabolisms. Furthermore, an analysis of amino acid concentrations and compositions in basement fluids support the notion that heterotrophic activity is ongoing. Similarly, the enrichment of acidic amino acids and depletion of hydrophobic ones relative to sedimentary particulate organic matter suggests that surface sorption and desorption also alters amino acids in the basaltic basement. In summary, although the oceanic basement aquifer is a net sink for deep seawater DOC, similar amino acid concentrations in basement aquifer and deep seawater suggest that DOC is preferentially removed in the basement over dissolved amino acids. Our data also suggest that organic carbon cycling occurs in the oceanic basaltic basement, where an active subsurface biosphere is likely responsible for amino acid synthesis and degradation.

Microbial life has been detected well into the igneous crust of the seafloor (i.e., the oceanic basement), but there have been no reports confirming the presence of viruses in this habitat. To detect and characterize an ocean basement virome, geothermally heated fluid samples (ca. 60 to 65°C) were collected from 117 to 292 m deep into the ocean basement using seafloor observatories installed in two boreholes (Integrated Ocean Drilling Program [IODP] U1362A and U1362B) drilled in the eastern sediment-covered flank of the Juan de Fuca Ridge. Concentrations of virus-like particles in the fluid samples were on the order of 0.2 × 105 to 2 × 105 ml−1 (n = 8), higher than prokaryote-like cells in the same samples by a factor of 9 on average (range, 1.5 to 27). Electron microscopy revealed diverse viral morphotypes similar to those of viruses known to infect bacteria and thermophilic archaea. An analysis of virus-like sequences in basement microbial metagenomes suggests that those from archaeon-infecting viruses were the most common (63 to 80%). Complete genomes of a putative archaeon-infecting virus and a prophage within an archaeal scaffold were identified among the assembled sequences, and sequence analysis suggests that they represent lineages divergent from known thermophilic viruses. Of the clustered regularly interspaced short palindromic repeat (CRISPR)-containing scaffolds in the metagenomes for which a taxonomy could be inferred (163 out of 737), 51 to 55% appeared to be archaeal and 45 to 49% appeared to be bacterial. These results imply that the warmed, highly altered fluids in deeply buried ocean basement harbor a distinct assemblage of novel viruses, including many that infect archaea, and that these viruses are active participants in the ecology of the basement microbiome., IMPORTANCE The hydrothermally active ocean basement is voluminous and likely provided conditions critical to the origins of life, but the microbiology of this vast habitat is not well understood. Viruses in particular, although integral to the origins, evolution, and ecology of all life on earth, have never been documented in basement fluids. This report provides the first estimate of free virus particles (virions) within fluids circulating through the extrusive basalt of the seafloor and describes the morphological and genetic signatures of basement viruses. These data push the known geographical limits of the virosphere deep into the ocean basement and point to a wealth of novel viral diversity, exploration of which could shed light on the early evolution of viruses.

The oceanic basaltic crust is the largest aquifer on Earth and has the potential to harbor substantial subsurface microbial ecosystems, which hitherto remains largely uncharacterized and is analogous to extraterrestrial subsurface habitats. Within the sediment-buried 3.5 Myr old basaltic crust of the eastern Juan de Fuca Ridge flank, the circulating basement fluids have moderate temperature (∼65 °C) and low to undetectable dissolved oxygen and nitrate concentrations. Sulfate, present in high concentrations, is therefore expected to serve as the major electron acceptor in this subsurface environment. This study focused on the availability and potential sources of two important electron donors, methane (CH4) and hydrogen (H2), for the subseafloor biosphere. High integrity basement fluids were collected via fluid delivery lines associated with Integrated Ocean Drilling Program (IODP) Circulation Obviation Retrofit Kits (CORKs) that extend from basement depths to outlet ports at the seafloor. Two new CORKs installed during IODP 327 in 2010, 1362A and 1362B, were sampled in 2011 and 2013. The two CORKs are superior than earlier style CORKs in that they are equipped with coated casing and polytetrafluoroethylene fluid delivery lines, reducing the interaction between casing materials with the environment. Additional samples were collected from an earlier style CORK at Borehole 1301A. The basement fluids are enriched in H2 (0.05–1.8 μmol/kg), suggesting that the ocean basaltic aquifer can support H2-driven metabolism. The basement fluids also contain significant amount of CH4 (5–32 μmol/kg), revealing CH4 as an available substrate for subseafloor basaltic habitats. The δ13C values of CH4 from the three boreholes ranged from −22.5 to − 58 ‰ , while the δ2H values ranged from −316 to 57‰. The isotopic compositions of CH4 and the molecular compositions of hydrocarbons suggest that CH4 in the basement fluids is of both biogenic and abiotic origins, varying among sites and sampling times. The δ2H values of CH4 in CORK 1301A fluid samples are much more positive than found in all other marine environments investigated to date and are best explained by the partial microbial oxidation of biogenic CH4. In conclusion, our study shows that CH4 and H2 are persistently available to fuel the deep biosphere and that CH4 is both produced and potentially consumed by microorganisms in the oceanic basement.

The permeable rocks of the upper oceanic basement contain seawater-sourced fluids estimated to be ~ 2% of the global ocean volume. This represents a very large potential subsurface biosphere supported by chemosynthesis. Recent collection of high integrity samples of basement fluid from the sedimented young basaltic basement on the Juan de Fuca Ridge flanks, off the coasts of Vancouver Island (Canada) and Washington (USA), and subsequent chemical analyses permit numerical modeling of metabolic redox reaction energetics. Here, values of Gibbs free energy for potential chemolithotrophic net reactions were calculated in basement fluid and in zones where basement fluid and entrained seawater may mix; the energy yields are reported both on a per mole electrons transferred and on a per kg of basement fluid basis. In pure basement fluid, energy yields from the anaerobic respiration processes investigated are anemic, releasing

The rock-hosted, oceanic crustal aquifer is one of the largest ecosystems on Earth, yet little is known about its indigenous microorganisms. Here we provide the first phylogenetic and functional description of an active microbial community residing in the cold oxic crustal aquifer. Using subseafloor observatories, we recovered crustal fluids and found that the geochemical composition is similar to bottom seawater, as are cell abundances. However, based on relative abundances and functional potential of key bacterial groups, the crustal fluid microbial community is heterogeneous and markedly distinct from seawater. Potential rates of autotrophy and heterotrophy in the crust exceeded those of seawater, especially at elevated temperatures (25 °C) and deeper in the crust. Together, these results reveal an active, distinct, and diverse bacterial community engaged in both heterotrophy and autotrophy in the oxygenated crustal aquifer, providing key insight into the role of microbial communities in the ubiquitous cold dark subseafloor biosphere.

The permeable upper oceanic basement serves as a plausible habitat for a variety of microbial communities. There is growing evidence suggesting a substantial subseafloor biosphere. Here new time series data are presented on key inorganic species, methane, hydrogen and dissolved organic carbon (DOC) in ridge flank fluids obtained from subseafloor observatory CORKs (Circulation Obviation Retrofit Kits) at Integrated Ocean Drilling Program (IODP) boreholes 1301A and 1026B. These data show that the new sampling methods ( Cowen et al., 2012 ) employed at 1301A result in lower contamination than earlier studies. Furthermore, sample collection methods permitted most chemical analyses to be performed from aliquots of single large volume samples, thereby allowing more direct comparison of the data. The low phosphate concentrations (0.06–0.2 μM) suggest that relative to carbon and nitrogen, phosphorus could be a limiting nutrient in the basement biosphere. Coexisting sulfate (17–18 mM), hydrogen sulfide (∼0.1 μM), hydrogen (0.3–0.7 μM) and methane (1.5–2 μM) indicates that the basement aquifer at 1301A either draws fluids from multiple flow paths with different redox histories or is a complex environment that is not thermodynamically controlled and may allow co-occurring metabolic pathways including sulfate reduction and methanogenesis. The low DOC concentrations (11–18 μM) confirm that ridge flank basement is a net DOC sink and ultimately a net carbon sink. Based on the net amounts of DOC, oxygen, nitrate and sulfate removed (∼30 μM, ∼80 μM, ∼40 μM and ∼10 mM, respectively) from entrained bottom seawater, organic carbon may be aerobically or anaerobically oxidized in biotic and/or abiotic processes.

A new analytical technique using inductively coupled plasma–quadrupole mass spectrometry (ICP-QMS) has been developed that produces permil-level precision in the measurement of uranium concentration ([U]) and isotopic composition (δ234U) in natural materials. A 233U-236U double spike method was used to correct for mass fractionation during analysis. To correct for ratio drifting, samples were bracketed by uranium standard measurements. A sensitivity of 6–7 × 108 cps/ppm was generated with a sample solution uptake rate of 30 μL/min. With a measurement time of 15–20 min, standards of 30-ng uranium produced a within-run precision better than 3‰ (±2 R.S.D.) for δ234U and better than 2‰ for [U]. Replicate measurements made on standards show that a between-run reproducibility of 3.5‰ for δ234U and 2‰ for [U] can be achieved. ICP-QMS data of δ234U and [U] in seawater, coral, and speleothem materials are consistent with the data measured by other ICP-MS and TIMS techniques. Advantages of the ICP-QMS method include low cost, easy maintenance, simple instrumental operation, and few sample preparation steps. Sample size requirements are small, such as 10–14 mg of coral material. The results demonstrate that this technique can be applied to natural samples with various matrices.