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

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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) sug- gest 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.
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