Abiotic Hydrogen (H2) Sources and Sinks Near the Mid-Ocean Ridge (MOR) with Implications for the Subseafloor Biosphere

Abiotic hydrogen (H2) sources and sinks near the Mid-Ocean Ridge (MOR) with implications for the subseafloor biosphere

Stacey L. Wormana,1, Lincoln F. Pratsona, Jeffrey A. Karsonb, and William H. Schlesingera,c,1 aDivision of Earth and Ocean Sciences, Nicholas School of the Environment, Duke University, Durham, NC 27708; bDepartment of Earth Sciences, Syracuse University, Syracuse, NY 13244; and cCary Institute of Ecosystem Studies, Millbrook, NY 12545

Contributed by William H. Schlesinger, April 1, 2020 (sent for review February 18, 2020; reviewed by Marvin Lilley and Kenneth H. Nealson)

Free hydrogen (H2) is a basal energy source underlying chemosyn- Juan de Fuca Ridge (JdFR), where subsurface microbes con- thetic activity within igneous ocean crust. In an attempt to system- sume ∼50 to 80% of H2 production (25), and on the Mid- atically account for all H2 within young oceanic lithosphere (<10 Atlantic Ridge (MAR), where consumption is ∼90% (26). Ma) near the Mid-Ocean Ridge (MOR), we construct a box model Our MOR-scale estimate is the result of a bottom-up analysis of this environment. Within this control volume, we assess abiotic that includes 19 different processes, more than half of which we 12 12 H2 sources (∼6 × 10 mol H2/y) and sinks (∼4 × 10 mol H2/y) and could not locate previous estimates for (Fig. 2). The type, ∼ × 12 then attribute the net difference ( 2 10 mol H2/y) to microbial quantity, and quality of published information available for these consumption in order to balance the H2 budget. Despite poorly processes vary dramatically; so, each estimate in our model is constrained details and large uncertainties, our analytical frame- surrounded by its own and often considerable uncertainties. H2 work allows us to synthesize a vast body of pertinent but cur- production from serpentinization, for instance, has been quan- rently disparate information in order to propose an initial global tified more than any other source and existing estimates range 10 12 estimate for microbial H2 consumption within young ocean crust from ∼10 to ∼10 mol H2/y (Table 1). Since similarly large that is tractable and can be iteratively improved upon as new data uncertainties are potentially associated with each of our estimates, and studies become available. Our preliminary investigation sug- we also conduct a sensitivity analysis wherein we vary the contri- gests that microbes beneath the MOR may be consuming a size- bution of an individual process to our box model by four orders of ∼ EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES able portion (at least 30%) of all produced H2, supporting the magnitude (plus or minus two orders of magnitude relative to our widely held notion that subseafloor microbes voraciously consume estimate) while holding all other model terms constant. In addi- ’ H2 and play a fundamental role in the geochemistry of Earth s tion to demonstrating that our ∼30% estimate represents a rather ocean–atmosphere system. robust lower boundary, understanding how individual estimates affect Hmicrobes is helpful context when considering previously biogeochemistry | origins of life | hydrogen | Mid-Ocean Ridge | microbes published estimates and prioritizing future work. Knowing how much H2 is available to fuel microbial activity lthough a growing body of evidence confirms the presence beneath the MOR allows us to explore the potential size and Aof chemosynthetic autotrophs within igneous oceanic crust, significance of this subseafloor biosphere. If energy is the first- the metabolism of the subseafloor biosphere remains largely order constraint on life, for example, our modeling results sug- unknown (1–4). Near the Mid-Ocean Ridge (MOR), free hy- gest primary production within young oceanic crust is at most 12 drogen (H2) is important to microbial communities and may ∼2 × 10 g C/y. Although notably small relative to the metabolism even be their basal energy resource (5–8). Knowing how much of the photosynthetic-based biosphere (∼1 × 1017 g C/y) (27), the H2 is available in this environment is therefore a key constraint modeled uptake of H2 by this chemosynthetic biome meaningfully on the potential activity of subseafloor life. suppresses the rate that H2 enters into our ocean–atmosphere Since the earliest discovery of H2 in deep-sea hydrothermal vents (9), our observational record has expanded considerably Significance but our understanding has remained limited. The different geologic sources and sinks of H2 near the MOR, for example, This paper estimates natural hydrogen production by various have never been inventoried and size estimates are either rare or geological processes and its ultimate fate in young oceanic nonexistent (Table 1). A global assessment of their collective, crust near the Mid-Ocean Ridge (MOR). Hydrogen is an im- total magnitude is also completely missing. Here we attempt to portant source of energy for microbes living beneath the sea- identify, describe, and quantify the various processes adding or < floor. Knowing how much is available to support these biological removing H2 from young oceanic lithosphere ( 10 Ma). Using a communities is therefore key to understanding the size and sig- box model and budgeting framework, we assume the net differ- − nificance of this biome, one of the potential first environments ence between all sources and sinks, Hsources Hsinks, represents for life on Earth and a potential environment for life on microbial available H2 (Fig. 1). other planets. Such an effort is confounded by the fact that this remote and relatively inaccessible geologic region is largely unexplored, Author contributions: W.H.S. designed research; S.L.W. performed research; J.A.K. con- sparsely sampled, and highly heterogeneous and by the com- tributed new reagents/analytic tools; S.L.W., L.F.P., J.A.K., and W.H.S. analyzed data; and plexities of the varied processes involved as well as their spatial S.L.W. and W.H.S. wrote the paper. and temporal variability (24). Given the many poorly constrained Reviewers: M.L., University of Washington; and K.H.N., University of Southern California. details and inherent uncertainties, we aim at a conservative order The authors declare no competing interest. of magnitude estimate for Hmicrobes that we derive from a lower- Published under the PNAS license. × 12 bound estimate for Hsources (6 10 mol H2/y) and an upper- 1To whom correspondence may be addressed. Email: [email protected] or schlesingerw@ 12 bound estimate for Hsinks (4 × 10 mol H2/y). Results suggest caryinstitute.org. 12 that Hmicrobes is at least ∼2 × 10 mol H2/y, an amount that This article contains supporting information online at https://www.pnas.org/lookup/suppl/ represents ∼30% of Hsources (Fig. 1). This seems to be a rea- doi:10.1073/pnas.2002619117/-/DCSupplemental. sonable lower boundary given studies of vent fields along the www.pnas.org/cgi/doi/10.1073/pnas.2002619117 PNAS Latest Articles | 1of11 Table 1. Existing published estimates of individual H2 sources generates H2 and a general statement of this notably complex and sinks, grouped by process and then ordered according to process is increasing size 2() FeO + H O → ()Fe O + H , [2] Process Estimate (mol H2/y) Ref. rock 2 2 3 rock 2

2+ Sources where (FeO)rock represents the ferrous (Fe ) component of × 12 3+ hcrys 6.3 10 10 igneous silicates and (Fe2O3)rock represents ferric-bearing (Fe ) – × 11 hserp 0.8 1.3 10 11 alteration minerals (30). Existing MOR estimates vary consider- × 11 11 1.67 10 12 ably from ∼0.8 to 49 × 10 mol H2/y (Table 1). We recently × 11 12 6.6 10 13 proposed an estimate of ∼1.2 × 10 mol H2/y, derived from 1.2 × 1012 14 a mechanistic model that integrates key aspects of the process 1.02–2.57 × 1012 15 with empirical data (14). Another recent analysis suggests that 4.9 × 1012 16 serpentinization along Oceanic Transform Faults may produce ± × 11 12 hwea 4.5 3 10 17 an additional ∼0.61 to 1.07 × 10 mol H2/y resulting in a com- × 10 12 hbslt 6 10 18 bined, total estimate of ∼1.02 to 2.57 × 10 mol H2/y (15). There Sinks may be some overlap between these numbers so we use ∼1 × 1012 × 11 off-l-um 4.6 10 12 mol H2/y for conservatism. × 11 12 9 10 18 Crystallization (hcrys = ∼3 × 10 mol H2/y). During late-stage crys- × 10 on-h-um 6.6 10 12 tallization, H2 production occurs as water dissolved within 7.7 × 1010 19 magma oxidizes ferrous iron (31), 9 × 1010 20 on-h-m 1.9–9.2 × 109 21 () + () → ()· + [3] 3 FeO magma H2O magma FeO Fe2O3 rock H2. 0.3–1.5 × 1010 22 10 0.4–1.8 × 10 23 Based on the annual volume of crystallizing magma (21 km3/y) 10 3.3 × 10 19 (32) and the amount of H that must be generated (301 mol H / 10 2 2 6 × 10 9 m3) to account for the autooxidation observed in paired samples Chronic venting estimates (i.e., nonacute) are abbreviated as Location of glassy rinds and Mid-Ocean Ridge Basalt (MORB) (31), Hol- ’ × 12 [on- or off-axis] − Temperature [high (h) or low (l)] − Host rock [mafic (m) loway and O Day (10) estimate production at 6.3 10 mol H2/y. 3+ or ultramafic (um)]. Observations of Fe /ΣFe in another paired sample (33) suggest about half as much autooxidation (SI Appendix, Table S1), which we prefer for conservatism. The extent to which this pro- system and therefore suggests an outsized impact of MOR mi- cess occurs at depth beneath the MOR, within crystallizing gab- crobes on geochemical cycling (28, 29). Our analysis is also rele- broic rocks, is hard to determine given how little is known about vant to other research topics across the Earth and planetary lower oceanic crust. It is also hard to make defensible general- sciences. We do not yet know what constrains life in this rather izations from the available data: gabbro samples recovered extreme environment, but the answer informs our conceptualiza- from the MOR come from a diverse suite of poorly constrained tion of life and our search for it in other intra- and extraterrestrial environments that are similarly removed or even completely iso- lated from the present-day biosphere. H2 is also important to the redox state of our ocean–atmosphere; so, our quantitative analysis is also relevant to theories surrounding secular changes in geological and/or geochemical parameters throughout Earth’shistory. Box Model In a steady-state box model of young oceanic lithosphere (<10 Ma), the amount of H2 available to lithospheric microbes, Hmicrobes,is

Hmicrobes = Hsources − Hsinks, [1] where Hsources and Hsinks represent the total rate that nonmicrobial (“abiogenic”) processes generate and remove H2, respectively (in moles of H2 per year). Below we identify and describe the various processes contributing to Hsources and Hsinks (Figs. 1 and 2) and briefly summarize previous estimates (Table 1). To arrive at a conservative net assessment of Hmicrobes,wecon- struct lower- and upper-bound estimates for all source (Table 2) and sink terms (Tables 3 and 4), respectively, and round all estimates to one significant figure. Additional details including ex- Fig. 1. Steady-state box model depicting H2 budget of young (<10 Ma) plicit calculations are provided in SI Appendix. ocean crust near the MOR. We construct a conservative, lower-bound esti- 12 mate for microbially available H2, Hmicrobes (2 × 10 mol H2/y), using a lower- 12 Estimates bound estimate for total abiogenic H2 production, Hsources (6 × 10 mol H2/y), 12 and an upper-bound estimate for sinks, H (2 × 1012 mol H /y) . At least H2 Sources (Hsources = ∼6 × 10 mol H2/y). At least nine different sinks 2 nine different processes contribute to Hsources (Fig. 2A and Table 2), and at abiogenic processes produce H2 within young oceanic crust least 10 different processes contribute to Hsinks (Fig. 2B), which we lump into (Fig. 3). two major categories, the H2 that 1) escapes into the ocean via hydrothermal = ∼ × 12 Serpentinization (hserp 1 10 mol H2/y). The hydration or ser- vents, hvented (Table 3) and 2) remains beneath the seafloor within crustal pentinization of ferrous minerals, typically olivine or pyroxene, pore waters and rocks, hremaining (Table 4).

2of11 | www.pnas.org/cgi/doi/10.1073/pnas.2002619117 Worman et al. AB

Fig. 2. Estimates of processes contributing to our lower-bound estimate of Hsources (A) and upper-bound estimate of Hsinks (B), along with previously published estimates where applicable (gray dots; plotted at midpoint for estimates with ranges) (Table 1). Chronic venting estimates (i.e., nonacute) are abbreviated as Location [on- or off-axis] − Temperature [high (h) or low (l)] − Host rock [mafic (m) or ultramafic (um)]. settings that generally lack geologic context and unlike MORBs, 20 Ma (17). Assuming that water causes 50% of the observed are compositionally diverse (34, 35). H2 production by intrusive oxidation and that only the top ∼0.5 km of nascent crust un- rocks should be larger than extrusive rocks, however, since the dergoes weathering, Bach and Edwards (17) estimate production 11 reaction (Eq. 3) 1) has more time to proceed given slower crys- at ∼4.5 ± 3 × 10 mol H2/y. Since alteration is generally limited tallization rates and 2) is H2O limited (10) and plutonic rocks to the margins of cracks and fractures, we adopt their lower- 11 typically contain more water. It is therefore conservative to assume bound value of ∼2 × 10 mol H2/y for conservatism. that autooxidation within plutonic rocks is similar to extrusive Middle and lower oceanic crust are less exposed but also undergo 12 ones, suggesting crystallization produces ∼3 × 10 mol H2/y (SI weathering. Gabbros recovered from active tectonic escarpments at Appendix,Eq.S2). fast-spreading ridges (e.g., Hess Deep, Pito Deep, Cocos, and possibly 10 EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES High-temperature basalt alteration (hbslt = ∼6 × 10 mol H2/y). During Oman), for example, are relatively young and generally <10% oxi- the high-temperature (∼350 to 400 °C) alteration of oceanic dized. Dredge samples and outcrops of middle and lower oceanic crust by seawater, the majority of ferrous silicates alter to ferrous crust on slower-spreading ridges are older and therefore tend to be iron minerals (e.g., chlorite, amphibole). A small number, how- more oxidized (>50%) (24, 35). Although less pervasive, such ever, alter to ferric-bearing minerals and produce H2 (36), weathering is rather widespread and provides further confidence that 11 ∼2 × 10 mol H2/y represents a lower bound. ()+ → + + [4] = ∼ × 11 3Fe2SiO4 rock 2H2O 3SiO2 2Fe3O4 2H2. Magmatic degassing (hmag 7 10 mol H2/y). H2 is also found in Carbon–Oxygen–Hydrogen (COH) magmatic systems, Although the depth to which hydrothermal fluids penetrate the oceanic crust is not known, limited sampling suggests that upper 2H2O + CH4 ⇌ 4H2 + CO2. [8] crust is pervasively altered whereas lower crust is mostly un- altered (24). Based on the total amount of FeO in the reactive At magmatic temperatures (∼1,200 °C), this equilibrium is displaced basaltic portion of oceanic crust, Sleep and Bird (18) note that strongly to the right, suggesting that H2 may be a component of 12 production could be as high as ∼3.75 × 10 mol H2/y but pro- magmas (38). Other theories appeal to H2 loss during the ascent of 10 pose a lower estimate of ∼6 × 10 mol H2/y based on the magmas to explain why basalt source regions are more reduced than Quartz–Fayalite–Magnetite equilibrium (Table 1). Adopting surface basalts (39), but we were unable to locate any estimates. their conservative approach and using own our estimate for the Popping rocks are MORBs with unusually high gas contents high-temperature hydrothermal fluid through axial mafic rocks that are thought to represent lava with no degassing history prior 12 suggests a production rate of ∼1 × 10 mol H2/y. Although more to eruption (40, 41). An early sample recovered from the MAR consistent with the rest of our analysis, we prefer the lower value 10 of ∼6 × 10 mol H2/y (18) for conservatism (SI Appendix,Eq.S3). We do not consider the potential for deeper alteration, but it is Table 2. Lower-bound estimates of the nine processes worth noting that some ophiolites contain rare high-temperature contributing to Hsources, ordered by size and broken down into alteration veins in gabbroic crustal sections (37); so, this process common terms (SI Appendix) could be more pervasive than our estimate embraces. Volumetric = ∼ × 11 Crustal weathering (hwea 2 10 mol H2/y). Oceanic crust is also Volume production Production altered by seawater as it cools and ages, forming lower-temperature 3 3 Process (km /y) (mol H2/km ) (mol H2/y) (<250 °C) ferric-bearing minerals and H2: for example (17), 11 12 hcrys 21 1.5 × 10 3 × 10 11 12 hserp 1.6 6.3 × 10 1 × 10 ()+ → ()+ [5] × 10 × 11 2 FeO rock 4H2O 2Fe OH 3 H2 hmag 21 3.1 10 7 10 7 4 11 hrad 1 × 10 5 × 10 5 × 10 h 0.7 2.3 × 1011 2 × 1011 2() FeO + 2H2O → 2FeOOH + H2 [6] wea rock 12 11 hlava 0.07 2.1 × 10 1 × 10 × 9 × 10 ()+ → + [7] hbslt 50 1.2 10 6 10 2 FeO rock H2O Fe2O3 H2. 9 10 hfrac 25 1 × 10 3 × 10 − h 3 × 10 8 3 × 1013 9 × 105 A compilation of Deep Sea Drilling Project and Oceanic Drilling pyrt Program samples suggests that crustal weathering occurs within Total (H )6× 1012 the extrusive rock layer and continues until crust ages to ∼10 to sources

Worman et al. PNAS Latest Articles | 3of11 Fig. 3. Diagram depicting young oceanic crust near the MOR and the nine different abiogenic H2-producing processes contributing to our lower-bound estimate of Hsources (Table 2). MOHO, Mohoroviciˇ c discontinuity.

11 exploded on deck prior to being analyzed, but fragments con- suggests that hlava is ∼1 × 10 mol H2/y (SI Appendix,Eq.S20) tained 0.881 mL/g of dissolved gases, of which 26.7% was H2 Seawater may also interact with extruding lava throughout the (40). These measurements suggest an estimate for hmag of ∼7 × body of a flow (e.g., usually confined to cooling cracks and/or 11 pillow margins) or even during explosive submarine events (49). 10 mol H2/y (SI Appendix, Eq. S12), which should be conser- The extent of such interactions is largely unknown but further vative given the likelihood that H2 was lost in the explosion prior suggests that our estimate for hlava is on the lower end. to this measurement. Although a recent expedition has sought to 10 Rock fracturing (hfrac = ∼3 × 10 mol H2/y). The fracturing of rock provide more comprehensive characterizations of popping rock ruptures chemical bonds, producing radicals that can react with volatiles (42), H2 content data have not yet been published. 11 water to produce H2 (50, 51), Radiolysis (hrad = ∼5 × 10 mol H2/y). Radiation released by decaying radioactive elements within oceanic rocks such as 2()≡ Si · + 2H2O → 2()≡ SiOH + H2. [11] uranium (238U and 235U), thorium (232Th), and potassium (40K) can excite and ionize water, producing free radicals that may lead We could not locate any previous estimates of this process within to the radiolysis of water (43, 44), young oceanic crust. Modifying a model that relates H2 to earthquake magnitude M (51) and considering earthquakes up 2H · → H2. [9] to M = 8, reflecting the largest recorded MOR event to date 10 (52), suggest that hfrac may be ∼3 × 10 mol H2/y (SI Appendix, MOR basaltic aquifer rocks may be producing ∼0.5 to 50 × 105 Eq. S24). This estimate is likely a lower bound for several rea- 3 mol H2/km per year depending on composition (e.g., concen- sons. First, larger earthquakes may occur at the MOR, and tration of radioactive elements) and fracture widths (44). Apply- considering events up to M = 9 triples production (∼9 × 1010 mol ing this lower-bound volumetric production rate to the extrusive H2/y) and up to M = 10 increases it by an order of magnitude ∼ × 7 3 11 layer of young oceanic crust, 1 10 km , suggests production (∼3 × 10 mol H2/y) (SI Appendix, Table S3). Second, the seismic 11 is ∼5 × 10 mol H2/y (SI Appendix, Eq. S14). record captures only a small fraction of all fracturing and faulting – = ∼ × 11 Lava seawater interaction (hlava 1 10 mol H2/y). The interaction near the MOR; most tectonic movements are aseismic (53). Al- – of seawater with extruding lava produces H2 (45 47), though less H2 is produced by small-scale fracturing (51), aseismic cataclastic deformation is pervasive and could produce significant () + () → ()+ [10] 2 FeO magma H2O seawater Fe2O3 rock H2. quantities of H2. 5 Pyrite formation (hpyrt = ∼9 × 10 mol H2/y). Stoichiometric yields of – Theextentoflavaseawater interaction is hard to determine, H2 have been observed during the inorganic formation of pyrite but seawater broadly interacts with the surface of extrusive (54, 55), flows as evidenced by fragmentation and quenched rinds. Com- bining volumetric extrusion rates at the MOR (48) with an FeS + H2S → FeS2 + H2. [12] assumption that flows are ∼1 m thick, we estimate a lava surface area of ∼7to50× 103 km2/y. Using the lower limit and assuming This reaction may be occurring at the high-temperature black seawater penetration is ∼1 cm, the stoichiometry of Eq. 10 smoker vents characteristic of the MOR; however, the pyrite

4of11 | www.pnas.org/cgi/doi/10.1073/pnas.2002619117 Worman et al. Table 3. Upper-bound estimates of the seven processes assign each to a specific venting style (Fig. 5) by combining data contributing to hvented, ordered by size and broken down into culled from these references with additional information from common terms (SI Appendix) the InterRidge Vents Database (59). We recognize that this is inherently imprecise: we assign a single rock type to each mea- Fluid flux [H2] Venting rate Vent type (kg/y) (mM) (mol H /y) surement, for example, but vents are often hosted in a mix of 2 mafic and ultramafic rocks and/or even sediments where bio- × 14 × 12 off-l-um 2 10 10 2 10 genic processes may be producing H2 (60). Our overarching goal, on-h-um 6 × 1013 10 6 × 1011 however, is to construct empirically informed estimate parame- × 13 × 11 Acute 1 10 40 4 10 ters and to honor notable relationships between H2 concentra- on-h-m 7 × 1014 0.4 3 × 1011 tions and different vent characteristics. Measurements tend to off-l-m 2 × 1016 1.8 × 10−3 4 × 1010 have a positive skew, and so, we characterize the concentration × 15 × 10 on-l-m 3 10 0.005 2 10 associated with different vent types using the median H2 con- on-l-um 2 × 1014 0.1 2 × 1010 centration from our binned dataset (Fig. 5). On-axis high-temperature venting represents the largest por- × 12 Total (hvented)3.410 tion of our deep-sea H2 record (Fig. 5). Previous estimates from 10 basalt-hosted vents are ∼0.19 to 6 × 10 mol H2/y and from Chronic venting estimates (i.e., nonacute) are abbreviated as Location ∼ × 10 − − ultramafic-hosted vents are 6.6 to 9 10 mol H2/y (Table 1). [on- or off-axis] Temperature [high (h) or low (l)] Host rock [mafic (m) or 3 ultramafic (um)]. A few of these estimates are tied to He or heat fluxes, but most are basedonhydrothermalfluidfluxestimates. Combining our upper- bound flow estimates with median H2 concentrations from high- and other metal sulfides found more broadly in seafloor and temperature mafic- (0.4 mM) and ultramafic-hosted (10 mM) vent 11 11 chimney deposits primarily precipitate from hydrothermal fluids waters suggests annual escape rates of ∼3 × 10 and ∼6 × 10 mol with representative chemical reactions (56) including H2/y, respectively (Table 3). H2 also enters the ocean on-axis via low-temperature (“dif- 2+ + → + + + [13] Fe 2H2S FeS2 H2 2H fuse”) vents (61). H2 measurements from these vents are com- paratively sparse but have a median concentration of ∼0.005 mM 10 and (Fig. 5), suggesting a venting rate of ∼2 × 10 mol H2/y (Ta- ble 3). We were unable to find similar measurements to char- + 2+ + Cu + Fe + 2H2S → CuFeS2 + 0.5H2 + 3H . [14] acterize ultramafic systems and simply note that, when high- and EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES low-temperature flows are both measured at the same site, H2 Using data on the total tonnage and distribution of massive concentrations of the former are roughly two orders of magni- − sulfides (57), we estimate a deposit formation rate of ∼3 × 10 8 tude larger than the latter (25, 62). Since high-temperature ul- km3/y (SI Appendix, Table S4). Assuming pyrite represents ∼75% tramafic flows are ∼10 mM, applying this assumption to low- of massive sulfides by weight, the stoichiometry of Eq. 13 suggests temperature ultramafic flows suggests a concentration of ∼0.1 mM 5 10 a production rate of ∼9 × 10 mol H2/y at the MOR (SI Appendix, and a venting rate of ∼2 × 10 mol H2/y (Table 3). Eq. S27). H2 also escapes into the ocean via off-axis vents, the most prominent example being Lost City where vents hosted by an 12 H2 Sinks (Hsinks = ∼4 × 10 mol H2/y). Next we consider the total Oceanic Core Complex (OCC) emit low-temperature (<90 °C) rate that H2 may be lost from the MOR subsurface via abiotic H2-enriched fluids from ultramafic rocks (63, 64). We found two “ ” 11 processes, Hsinks (moles of H2 per year), where we define a sink previous estimates, ∼4.6 × 10 mol H2/y based on heat fluxes 11 as any process that effectively makes some portion of Hsources (12) and ∼9 × 10 mol H2/y based on fluid fluxes (18) (Table 1). unavailable to subseafloor microbes. Our review of the literature Measurements of H2 from Lost City vent waters are limited but suggests two major sink categories, range from <1 to 15 mM (63) and have a median value of 9 mM (Fig. 5). Although we do not currently know how commonplace = + [15] Hsinks hvented hremaining, Lost City-type venting is, combining this concentration with our off-axis ultramafic fluid flow estimate suggests an upper-bound 12 where hvented represents the rate that H2 enters the ocean via escape rate of ∼2 × 10 mol H2/y (Table 3). hydrothermal vents and hremaining represents H2 retained in the In addition to OCCs, H2 may be escaping off-axis from the MOR aquifer and rocks. fault bounded abyssal hills typical of fast-spreading centers (65). = ∼ × 12 Vented H2 (hvented 3 10 mol H2/y). A growing number of ob- It is unclear how widespread such flows may be, as so little of the servations confirm deep-sea hydrothermal venting of H2 (Fig. 4), seafloor has been investigated away from spreading centers. Such but quantifying this output is difficult given the significant spatial vents have seldom been seen or characterized but are likely to be and temporal heterogeneities of crustal accretion and hydrother- very significant for oceanic hydrothermal circulation and heat mal venting (24). A number of papers estimate H2 venting at the loss (66). Since we could not find relevant H2 measurements, we MOR but typically consider only one type of venting (e.g., high- temperature mafic venting) (Table 1). We begin by classifying the established diversity of hydrothermal venting, with flows that are either chronic (lasting years to decades) or acute (days to months) Table 4. Upper-bound estimates of the three processes and with other notable differences due to location (on or off axis), contributing to hremaining, ordered by size and broken down into temperature (high or low), and host rock (mafic or ultramafic) common terms (SI Appendix) (58). Although the partitioning of such flows remains poorly Volume [H2] Trapping rate 3 3 constrained and actively debated, combining what is known about Remaining (km /y) (mol H2/km ) (mol H2/y) hydrothermal fluid fluxes with other available estimates allows us Gabbros 15 1 × 1010 2 × 1011 to establish upper-bound fluid flow estimates for these different × 10 × 11 types of vents (Table 3 and SI Appendix,Eqs.S29–S35). Basalts 6 1.7 10 1 10 Pore waters 1.5 2 × 105 3 × 105 To characterize the H2 concentration of fluids associated with each, we compiled published data (Dataset S1). We found over 11 Total (hremaining)3× 10 ∼500 measurements of H2 in MOR vent waters (Fig. 4B) and

Worman et al. PNAS Latest Articles | 5of11 A

Fig. 4. Observations of H2 in MOR hydrothermal fluids (Dataset S1). (A)H2-enriched vent fluids have been reported on fast- to slow-spreading ridges including the East Pacific Ridge (EPR), Galapagos Spreading Center (GSC), JdFR (JdF), Gorda Ridge (GR), Central Indian Ridge (CIR), Gulf of California Rift Zone (GCRZ), Northern and Southern MAR (N. MAR and S. MAR, respectively), Mid-Cayman Rise (MCR), Mohns Ridge (MR), Red Sea (RS), and Southwest Indian Ridge (SWIR). Vent fields are ordered by ridge spreading rate, from superfast (EPR) to ultraslow (SWIR), with numbering displayed below. (B) There have been more than 500 measurements published in the literature, with H2 concentrations that span many orders of magnitude. Gray dots represent measure concentrations, white dots represent end-member concentration, and black dots represent observations not explicitly reported as either.

rely on the maximum pore water H2 concentration (∼1.8 μM) of H2 in crustal pore waters is relatively difficult and uncommon but off-axis mafic basement (67) to estimate an escape rate of ∼4 × basement fluids collected on the JdFR have H2 concentrations 10 ∼ μ 10 mol H2/y (Table 3). that range from 0.05 to 1.8 M (67). We do not know if these Lastly, we briefly consider acute venting since hydrothermal concentrations are representative of typical pore waters, but ap- vents and plumes become significantly enriched in H2 following plying the maximum concentration of 1.8 μM to the extrusive volcanic eruptions (68–70). Obtaining samples during or imme- basaltic aquifer (down to ∼0.5 km beneath the seafloor since diately following an eruption, when H2 concentrations are apt to crustal porosities approach “zero” at deeper crustal depths) sug- 5 be the highest, is difficult; so, we simply combine the largest gests a retention rate of ∼3 × 10 mol H2/y (Table 4 and SI Ap- posteruption H2 concentration measured to date at an MOR pendix,Eq.S36). vent (∼40 mM) (69) with an upper-bound estimate of the acute Some H2 may also remain beneath the seafloor inside MOR venting fluid flux, ∼1 × 1013 kg/y (SI Appendix, Eq. S35), to es- rocks as fluid inclusions, dissolved in fluids along mineral grain 11 timate an input to the ocean of ∼4 × 10 mol H2/y (Table 3). boundaries, and in situ within minerals. Obtaining rock H2 11 Remaining H2 (hremaining = ∼3 × 10 mol H2/y). Finally, we consider the contents requires rather specialized instruments and analyses rate at which H2 may be retained beneath the seafloor, hremaining, (71), so measurements are limited. Rock-crushing experiments within crustal pore waters and rocks. Considerably less literature of basalts, for example, report concentrations of ∼0.15 to 170 × 8 3 addresses this topic and we found no previous estimates, so this 10 mol H2/km (72) and suggest trapping within basalts could be 11 model component involves the largest uncertainties. Sampling for as high as ∼1 × 10 mol H2/y (Table 4 and SI Appendix,Eq.S38).

6of11 | www.pnas.org/cgi/doi/10.1073/pnas.2002619117 Worman et al. 11 gabbroic rocks are both ∼10 mol H2/y, and within basaltic pore 5 waters, it is ∼10 mol H2/y (Fig. 2B). Our conservative lower-bound estimate for microbially available H2, Hmicrobes, based on the net difference between our 12 lower-bound estimate of Hsources (∼6 × 10 mol H2/y) and upper- 12 12 bound estimate of Hsinks (∼4 × 10 mol H2/y), is ∼2 × 10 mol H2/y or equivalently, ∼30% of Hsources (Eq. 1 and Fig. 1). Although significant uncertainties surround the many terms contributing to this result, a sensitivity analysis suggests that this is a relatively robust lower boundary: Hmicrobes remains at ∼30% or else increases as we allow the size of a specific source or sink to vary across four orders of magnitude (two orders of magnitude on each side of our estimates) while holding all other model terms constant (Fig. 6). We elaborate on this point and address the few exceptions, where Hmicrobes drops to as low as zero, in our discussion. Fig. 5. Distribution of 500+ MOR H2 measurements, binned by venting type. We classified each measurement (Dataset S1) based on location rela- Discussion tive to the MOR (on- or off-axis, with plots representing on-axis locations minus the one labeled exception), temperature (high or low, demarcated at This undertaking represents an initial attempt to estimate how ∼100 °C), and host rock [mafic or ultramafic, based on information available much H2 is available to microbes living beneath the MOR. Our from the InterRidge Vents Database (59)]. Distribution of existing mea- bottom-up analysis also reflects an initial attempt to systemati- surements, along with basic information including sample size (n) and mean cally account for all of the sources and sinks of H2 within young (x) and median (x~) concentration (mM), for each group helps inform our oceanic crust (<10 Ma) and includes many processes that have estimates of H2 escaping to the ocean via different types of hydrothermal not previously been quantified (Fig. 2). Such an effort is con- vents (Table 3). founded by the fact that this remote and relatively inaccessible geologic region is largely unexplored, sparsely sampled, and We were unable to find similar measurements for gabbros, but the highly heterogeneous and by the complexities of the varied processes involved as well as their spatial and temporal vari- notably high CH4 content of plutonic oceanic rocks may form

ability (24). Although many unknowns and large uncertainties EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES upon cooling as the COH equilibrium (Eq. 8) shifts toward the left surround the individual terms and collective estimates we pre- at lower temperatures (73, 74). Unable to find measurements of sent, constructing an H2 budget of the MOR (Fig. 1) helps clarify MOR gabbros, we rely on recently published data from an what is known, identify where gaps exist, and highlight topics for ophiolite (75) to estimate an upper limit on the H2 content of future work. ∼ × 10 3 plutonic rocks of 1 10 mol H2/km and an occlusion rate of Although unable to find other existing estimates for compar- ∼ × 11 S41 2 10 mol H2/y (Table 4 and SI Appendix,Eq. ). ison, our conservative approach combined with model sensitivity Results together suggests that our assessment of Hmicrobes is a reasonable lower boundary. We consistently make assumptions that, for Our conservative, lower-bound estimates for the nine different example, result in a lower-bound estimate for H and fur- ∼ 5 ∼ 12 sources H2 production processes vary considerably, from 10 to 10 ther reducing individual source estimates does not meaningfully mol H2/y (Fig. 2A), and together suggest MOR production, lower Hmicrobes (Fig. 6A). The one exception, however, is crys- ∼ × 12 Hsources, totals 6 10 mol H2/y (Table 2). The largest sources tallization. This is the largest source in our model and decreasing are crystallization and serpentinization, with production magni- it reduces Hmicrobes, which approaches zero as crystallization ∼ 12 tudes of 10 mol H2/y, followed by magmatic degassing, radi- approaches the rate where Hsources equals Hsinks. We also con- olysis, crustal weathering, and lava–seawater interaction at ∼1011 sistently make assumptions to arrive at an upper-bound estimate mol H2/y. Production from high-temperature basalt alteration for Hsinks and further increasing these underlying estimates 10 and rock fracturing are both on the order of ∼10 mol H2/y, similarly decreases Hmicrobes (Fig. 6B). Although we cannot 5 whereas production from pyrite formation is ∼10 mol H2/y eliminate the possibility that Hmicrobes is even lower than we es- (Fig. 2A). timate, it is important to recognize that such a result requires There are at least 10 different nonmicrobial H2 sinks that we making our end-member assumptions even more extreme and consider in two major categories: H2 escaping the seafloor via would also be inconsistent with the widely held notion that lithospheric microbes beneath the MOR voraciously consume H hydrothermal vents, hvented, and H2 remaining beneath the sea- 2 (2, 7, 8, 25, 26, 68). Model sensitivity highlights that Hmicrobes floor in the MOR aquifer and rocks, hremaining (Fig. 2B). Our upper-bound estimate of h is ∼3.4 × 1012 mol H /y (Table 3), increases as we relax our end-member assumptions and allow the vented 2 parameter space for our model processes to become more an order of magnitude larger than we estimate for hremaining (∼3 × 1011 mol H /y) (Table 4), and together suggest a total loss, H , reasonable (Fig. 6). 2 sources Our assessment also seems conservative in light of a couple of of ∼4 × 1012 mol H /y. The largest sink is off-axis venting from 2 unique field studies that directly assess microbial H consump- low-temperature ultramafic-hosted vents at ∼1012 mol H /y, fol- 2 2 tion at the MOR. Evidence collected from sites on the JdFR lowed by acute venting and on-axis high-temperature mafic- and ∼ 11 (Endeavor and Mothra) and the MAR (Lost City) suggests that ultramafic-hosted vents at 10 mol H2/y. All other types of ∼ ∼ 10 subseafloor microbes consume 50 to 80% (25) and 90% (26) venting are ∼10 mol H2/y (Fig. 2B). At a coarser level, lumping of all H2, respectively. There are at least two potential expla- these flows and ignoring their overlap suggest the largest losses 12 11 nations for the sizable discrepancy between our analysis and from vents that are chronic (∼10 vs. ∼10 from acute vents), low these field studies. First, given our conservative approach, it is ∼ 12 ∼ 11 temperature ( 10 vs. 10 from high-temperature vents), and certainly possible that Hmicrobes is too low because we have ∼ 12 ∼ 11 ultramafic-hosted ( 10 vs. 10 from mafic-hosted vents). On- underestimated Hsources, overestimated Hsinks, or both, and using and off-axis vents are roughly equivalent in magnitude (both are conceivably higher source estimates or lower sink estimates re- ∼ 12 10 mol H2/y) (Table 3). We found considerably less literature sults in an estimate for Hmicrobes that is more in line with these field on hremaining but the magnitude of trapping within basalt and studies (Fig. 6). The second possibility is that these field-scale

Worman et al. PNAS Latest Articles | 7of11 A

Fig. 6. Sensitivity analysis showing relationship between individual (A) source and (B) sink estimates and Hmicrobes. Black dots represent our estimates and gray dots represent previously published estimates (Table 1). Horizontal dotted lines represent our final estimate for microbial consumption (Eq. 1)(∼30% of

Hsources), which is consistently lower than our estimates for individual processes due to final rounding of all numbers to one significant digit. Black lines show how Hmicrobes changes if we were to vary individual process estimates, while vertical dotted lines mark estimates that are either smaller or larger than our estimates by one or two orders of magnitude. Chronic venting estimates (i.e., nonacute) are abbreviated as Location [on- or off-axis] − Temperature [high (h) or low (l)] − Host rock [mafic (m) or ultramafic (um)]. studies (25, 26) are not representative of microbial consumption Conducting similar in-depth analyses of the many other pro- globally, suggesting a need to construct subseafloor H2 budgets cesses considered here would certainly complement this broader at different scales. Although pyrite formation contributes negli- effort and is key for gaining confidence about the size and rel- gibly to Hsources, for example, it represents the most concentrated ative importance of the various processes at play. The informa- ∼ 13 3 source of H2 in our model (e.g., 10 mol H2/km rock) (Ta- tion available on each process varies considerably, however, and ble 2) and may therefore be far more important for local mi- only a few appear large enough to meaningfully affect H crobial communities than its global magnitude alone seems to 2 availability at the MOR scale (Fig. 6). More in-depth studies suggest (Fig. 1). would therefore have to suggest rates that are orders of magni- We see a number of important areas for future work. While our observational record of the MOR is unarguably limited, we tude different from what we estimate to have first-order impacts have nonetheless amalgamated a rather expansive body of lit- on our modeling results (Fig. 6). Constructing top-down estimates would also complement this bottom-up analysis. Rates of erature that can be better leveraged. The H2 produced by serpentinization, for example, is relatively well studied at small deep-water O2 depletion, for example, suggest that hvented can be 13 scales (e.g., rock sample and vent field), and we previously used no larger than ∼10 mol H2/y (SI Appendix, Eq. S43), and since this body of work to quantify the process along the MOR (14). the vast majority of H2-producing processes involve the oxidation

8of11 | www.pnas.org/cgi/doi/10.1073/pnas.2002619117 Worman et al. of reduced iron, the redox balance of oceanic crust could simi- oxidation of globally significant quantities of reduced gases that larly help constrain Hsources. are otherwise kinetically inhibited at the low temperatures and Knowing how much H2 is available to microbes beneath the pressures characteristic of Earth’s surface, microbes help main- MOR, Hmicrobes, allows us to explore the potential size and sig- tain the present chemistry and conditions of our ocean– nificance of this subseafloor biosphere. Assuming microbes are atmosphere system (28, 29, 86). H2 fueled and energy limited (6, 76, 77), biomass (CH2O) for- Beyond the MOR, quantitative estimates of H2 help elucidate mation is directly proportional to Hmicrobes with the fixation of how different geologic settings compare in terms of their ability carbon dioxide (“anabolism”), to support life. Radiolysis, for example, is only ∼10% of Hsources in our box model (Fig. 1) but figures prominently in research on CO2 + 2H2 ⇌ CH2O + H2O, [16] lower-energy subsurface environments including older regions of igneous oceanic crust, deep-sea sediments, and within conti- consuming 2 mol H2 (29). Since some portion of Hmicrobes is used nental crust (43, 82, 87). A quick assessment suggests that radi- for cellular maintenance and growth (“catabolism”), primary olysis within older oceanic crust (>10 Ma) may be at least ∼8 × 12 production, Pmicrobes (moles of CH2O per year), is 10 mol H2/y (SI Appendix, Eq. S46) with the H2 trapped in MOR basalts and gabbros, ∼3 × 1011 mol H /y (Table 3), repre- = [17] 2 Pmicrobes k(0.5Hmicrobes), senting another potentially important source of energy. This relatively more expansive region of oceanic crust therefore appears where k denotes the partitioning of Hmicrobes between anabolic to have a comparable, and potentially even greater, amount of H2 and catabolic activities. While unknown for microbes beneath for supporting microbial communities, and this possibility could be the MOR, k is ∼0.2 in environments hospitable to life (78) and further explored by constructing a similar box model for this other should decrease in more extreme environments, as increasingly marine environment. At an even coarser scale, it is unclear if H2 harsh conditions force organisms to devote a larger portion of production is larger within oceanic or continental crust. Relatively their energy resources to catabolic activities. Assuming a value recent work focused on Precambrian crust, an area that represents for k of ∼0.2, however, places an upper limit on the productivity ∼70% of continental lithosphere, estimates total production at 17 11 of this biome and when used in solving Eq. , suggests a max- ∼0.36 to 2.27 × 10 mol H2/y (82). At the time of publication, this ∼ × 11 ∼ × 12 imum for Pmicrobes of 2 10 mol CH2O/y or 2 10 g C/y. estimate was similar in magnitude to available estimates from 11 Rather than energy, lithospheric MOR microbes may be oceanic lithosphere (∼10 mol H2/y) and therefore suggested constrained by other factors such as temperature, nutrients, al- parity. Here we focus on young oceanic lithosphere, an area that kalinity, pressure, or space (79, 80). Life does not thrive above represents only ∼10% of oceanic lithosphere globally, and esti- EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES ∼ 12 120 °C, for example, and the size of a temperature-limited mate total production at ∼10 mol H2/y. H2 is observed in other 17 subseafloor biosphere has been estimated at ∼2 × 10 gC marine settings including subduction zones, ocean–continent (79). This possibility suggests a much lower rate for Pmicrobes of transitions, and back arc spreading centers (88, 89), underscoring ∼ × 7 ∼ × 8 S44 5 10 mol CH2O/y or 6 10 g C/y (SI Appendix, Eq. ). the possibility that oceanic lithosphere dominates geologic H2 If these microbes consume all of the H2 that we estimate is production globally (14). = ∼ × 12 17 available to them (Hmicrobes 2 10 mol H2/y), solving Eq. The MOR H2 budget has probably varied throughout Earth’s suggests a value for k of 0.0005 (for every 1 mol H2 devoted to history as driven by secular changes in geological and/or geo- × 3 anabolism, 20 10 mol H2 are devoted to catabolism), and the chemical parameters. The abundance of H2 in the Archean at- apparent abundance of H2 would certainly help explain the mosphere, for example, suggests a different source/sink balance survival of life beneath the MOR where temperatures, pressures, (13). The ratio of oceanic to continental lithosphere was much and pH are elevated and nutrient availability is low. If these larger throughout this eon and elevated global heat loss was > microbes are not fully consuming Hmicrobes (i.e., k 0.0005), it probably also accommodated by higher rates of seafloor forma- becomes unclear how then to account for the remaining H2 tion or by a greater length of MOR plate boundaries (90). It surplus. One possibility is that at least some fraction, over geo- seems possible that crystallization, the largest H2 source in our logic time, has been structurally/stratigraphically trapped in the model, was even larger in the past with less production by ser- subsurface to form natural H2 gas reservoirs (81). While still pentinization due to increased magmatism and a more reduced speculative, naturally occurring gas accumulations featuring high Archean ocean. If such fluctuations in the MOR H budget were > 2 H2 contents ( 50%) and aquifer fluids enriched in dissolved H2 significant, they may have played a role in secular changes in (up to 7.4 mM) have been discovered in continental settings (82, atmospheric and/or oceanic chemistry (91). 83), and oceanic lithosphere remains largely unexplored. H2 is also central to many hypotheses surrounding the origin Whether we assume energy (∼1012 g C/y) or temperature and evolution of life (10, 18), so an improved understanding of ∼ 8 ( 10 g C/y) is the first-order constraint on life, the productivity lithospheric H2 may aid our search for extraterrestrial life. If of chemosynthetic MOR microbes appears relatively limited crystallization has the largest potential to produce H2, as our compared with photosynthesis. Primary production on modern analysis suggests, H2 may be most abundant on planetary bodies Earth, for example, is ∼1 × 1017 g C/y (27), and was ∼4 × 1014 g with active silicate magmatism (e.g., Venus, Io, and possibly on C/y by early anoxygenic phototrophs (11). Although relatively Europa, Titan, and Enceledus) and then become much more small in size, our box model suggests that MOR microbes limited when it is over (e.g., the Moon, Mars, and possibly nonetheless have an outsized influence on our planet’s global Mercury) (92). The lack or freezing of other fluids such as water biogeochemistry (28, 29). Imagine if these communities did not would impose additional constraints on the rate at which abiotic exist. Without subseafloor microbes consuming a sizable portion processes could add or remove H from the lithosphere, altering ∼ 2 (at least 30%) of MOR H2 production, the rate that this highly H2 availability in the primordial subsurface. Combining knowl- diffusive gas escapes into the ocean, hvented, would conceivably edge about ambient energy (H2) resources with other key theo- ∼ × 12 increase to 5 10 mol H2/y. Without deep-sea microbes in retical constraints on life, such as excessively high or low turn scavenging this H2 (84), it would then enter the atmosphere. temperatures, may therefore help us target our search for life Such an input represents a nonnegligible contribution (∼10%) to across the universe on other celestial bodies. 13 the atmospheric H2 budget, where sources total ∼10 mol H2/y, and therefore implies greenhouse and temperature effects (85). Data Availability. Data used in this analysis are provided in This insight is strikingly similar to those derived from meth- Dataset S1. Documentation of calculations for all estimates is ane (CH4) budgets of continental margins; by catalyzing the provided in SI Appendix.

Worman et al. PNAS Latest Articles | 9of11 ACKNOWLEDGMENTS. This research did not receive any specific grant and tectonic processes along MOR plate boundaries. We thank Paul Baker, from funding agencies in the public, commercial, or not-for-profit sectors. Tom Darrah, and Emily Klein for early conversations and input on J.A.K. acknowledges prior support by the NSF for studies of magmatic this work.

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