Anaerobic oxidation of methane by Mn oxides in sulfate-poor environments

Mn- and Fe-dependent AOM has been suggested to have the oxidative potential to oxidize a large amount of biogenic methane produced in the Proterozoic oceans (e.g., Beal et al., 2009). Yet, ¹²C- and Mn-rich carbonates in the rock records (e.g., Neoproterozoic and Mesoarchean Mn-rich rocks) were widely described to be a result of the organoclastic Mn-oxide reduction (Liu et al., 2006; Ossa Ossa et al., 2018) or of meteoric water diagenesis in nonmarine sandstones as seen in both the San Joaquin (California, USA) and Junggar (northwestern China) Basins (Hayes and Boles, 1993; Jin et al., 2008). Only one exception from the Jurassic Franciscan Complex, California Coast Ranges, was reported to directly relate to Mn-dependent AOM (Hein and Koski, 1987).

More recently, high-Mn calcites with δ¹³C_VPDB (VPDB—relative to Vienna Peedee belemnite) as low as −70‰ in the Mahu Sag (northwestern Junggar Basin in northwestern China), have been viewed to originate from thermochemical Mn reduction (TMnR) by thermogenetic methane at temperatures >95°C (Hu et al., 2018). The high temperatures were estimated with the assumption that the low-δ¹⁸O calcites were precipitated from evolved fresh water with δ¹⁸O_VSMOW (VSMOW—relative to Vienna standard mean ocean water) of −4‰ to −6‰. Such low-δ¹⁸O calcites have been, however, reported from low-temperature carbonates worldwide, e.g., Ediacaran cap dolostones (Zhao and Zheng, 2015), challenging the link between low δ¹⁸O value in calcite and high-temperature conditions. A new technique of multiply substituted isotopologues in carbonates, or “clumped isotopes”, can be used as an independent tool to estimate paleotemperatures and reconstruct initial fluid δ¹⁸O values (Ghosh et al., 2006; Staudigel and Swart, 2019). However, anomalously low clumped isotope values (Δ₄₇) have been reported from modern seep authigenic carbonates, formed by AOM coupled with sulfate reduction, corresponding to temperatures as much as 50°C warmer than ambient temperatures (Loyd et al., 2016). Thus, in such cases, the maximum temperatures can be constrained using clumped isotopes.

We use clumped isotopic data, in situ δ¹³C and δ¹⁸O values, and Mn contents of calcites to investigate possible roles of Mn(III/IV) (oxidation states of Mn) in the formation of high-Mn calcites, and, potentially, in the removal of biogenic methane from early Earth's oceans with low sulfate concentrations, where sulfate-dependent AOM may not have been efficient.

The Mahu Sag is located in the northwestern Junggar Basin, and petroleum is produced from the Lower Triassic Baikouquan Formation (unit T₁b, Fig. 1A). The Baikouquan Formation consists of alluvial fan-delta facies interlayered with massive, brown, silty mudstones and sandy to pebble conglomerates. The weathering of source mafic-ultramafic igneous rocks provided abundant high-valence Fe-Mn oxides to the basin, which were then deposited in the Baikouquan Formation (Hu et al., 2018). The Baikouquan Formation was buried to depths of 2500–5000 m and experienced compaction, two generations of calcite cementation, and dissolution of early calcite and feldspar (Zhang et al., 2018). Oil and the associated gas were charged from the Lower Permian unit P₁f mudstones into the Baikouquan Formation during two periods: the Early Jurassic and Early Cretaceous (Fig. 1B; Cao et al., 2015; Qi et al., 2015).

We examined thin sections of sandy conglomerates using transmitted-light and cathodoluminescence microscopes, a scanning electron microscope equipped with an energy-dispersive X-ray spectrometer, and an electron microprobe analyzer. Mineral identification and abundances were determined by powder X-ray diffraction. Iron oxides were identified by visible diffuse reflectance spectrum. Bulk-rock C-O isotopes and clumped isotopes were analyzed with a Thermo Finnigan MAT 253 mass spectrometer. We measured in situ carbon isotopes using a SHRIMP SI (sensitive high-resolution ion microprobe–stable isotope) secondary ion mass spectrometer (SIMS) with an error better than ±0.50‰. All δ¹³C and δ¹⁸O values are reported relative to VPDB and VSMOW, respectively. For detailed descriptions of the samples and methods, see the Supplemental Material¹.

Petrological observations indicate that the main diagenetic events include (1) compaction; (2) cementation of kaolinite, zeolite, and early calcite; followed by (3) dissolution of feldspar, volcanic detritus, zeolite, and early calcite; and finally (4) late calcite and quartz cementation (Fig. S1 in the Supplemental Material). The early calcites are 0%–15% in content and show poikilotopic features characteristic of less compaction due to shallow burial (Fig. 2A), and contain dissolution pores due to subsequent fluid influx. These calcites have MnO contents of 0.8 ± 0.01 wt% to 9.2 ± 0.01 wt% (1σ) with an average of 3.29 ± 2.72 wt% and a mean FeO/MnO ratio of 0.05 ± 0.03 (n = 40), and may have precipitated at temperatures <65°C as indicated by the clumped isotopes (n = 2; Fig. 3A; Table 1). Except for sample Ma154–3028.63, the remaining early calcites have in situ δ¹³C values ranging from −29.4‰ ± 0.5‰ to −58.1‰ ± 0.5‰ (1σ; n = 40; Table S1), showing a positive correlation with MnO contents (Fig. 3B). By comparison, late calcites, 0%–3% in MnO content, do not show dissolution but contain some oil fluid inclusions (Figs. 2B and 2C) and were precipitated at temperatures <142°C according to the clumped isotope data (n = 3; Table 1). These late calcites, which show higher FeO/MnO ratios compared to the early calcites, with an average of 0.23 ± 0.23 (n = 14), have much higher bulk δ¹³C, from −8.4‰ ± 0.1‰ to −6.0‰ ± 0.1‰ (1σ). Interestingly, iron oxides occur in both sandy conglomerate and interlayered mudstone, associated with detrital clay minerals (Figs. 2D and 2E), and have MnO/FeO ratios from 0.03 to 0.11 with an average of 0.04 ± 0.03 (n = 9; Table S2).

The produced elemental sulfur can be further oxidized to sulfate, which then fuels the sulfate-driven AOM. By conducting a simple thermodynamic calculation, we assessed the viability of this pathway in oxidizing methane versus the direct methane oxidation using Mn oxides (Ettwig et al., 2016). Using Gibbs free energy values for Mn oxides, sulfide, Mn(II), and water, and considering a range of values for concentration of different compounds in the anoxic ancient oceans, our results indicate a higher favorability of the direct Mn oxidation in comparison with the indirect pathway using sulfide and elemental sulfur (Fig. S2; Table S3). More precisely, our estimation indicates that even at tens of micromolar of sulfide concentration, the energy available through direct oxidation of methane using Mn oxide is approximately three times higher than that provided by the indirect pathway (Fig. S2). While the sulfur-involved indirect pathway is thermodynamically less favorable, the kinetics of such a pathway might be faster (Beal et al., 2009). For instance, previous experimental results indicate that despite the high energy available through direct Mn-driven AOM, the rate of sulfate-driven AOM is noticeably higher (Beal et al., 2009). Such a high rate, however, may have been substantially hampered at low sulfate concentrations, suggesting a less important role of the indirect pathway for methane oxidation. At the same time, in the studied area, sulfate reduction may have played only a minor role, if any, in the sedimentary sulfur cycle. This can be supported by two lines of evidence: (1) an absence of pyrite, as reported in Zhang et al. (2018) and Hu et al. (2018) as well as from all 15 conglomerate samples of this study, and (2) the fact that the calcites were precipitated earlier than the charge of oils (Fig. S1), and some of the calcites are not associated with oils. Taken together, by comparison with the direct methane oxidation using Mn oxides, the role of indirect oxidation of methane by Mn oxides using sulfur compounds under low sulfate conditions may have been insignificant, though it cannot be ruled out completely.

Our results further suggest that the iron-dependent oxidation of methane would have not been important in methane oxidation. More specifically, the calcites contain low FeO but high MnO contents, and thus were most likely generated from direct reduction of Mn(III/IV) by methane, with only a minor contribution from Fe(III).

It is crucial to determine whether biogenic oxidation of methane by Mn oxides occurred at low temperatures by microorganisms (Hein and Koski, 1987) or was thermochemical at slightly higher temperatures (Hu et al., 2018). Here, we present several lines of evidence for the occurrence of biogenic methane and its oxidation by Mn oxides at low temperatures to generate extremely ¹³C-depleted and Mn-rich calcites with high clumped isotope values (∆₄₇).

Triassic gas from the Mahu Sag has δ¹³C₁ (C₁—methane) values from −39.3‰ to −46.9‰ (Cao et al., 2015). On the 1/n–δ¹³C_n diagram (n is carbon number of a gas molecule) of Chung et al. (1988), all the current δ¹³C₁ values are significantly lower than for the co-generative, unaltered gas of the model for the Baikouquan Formation gas (Fig. S3). This implies that thermogenic gas must have mixed with biogenic methane (δ¹³C₁ <−50‰; Whiticar, 1999), and the biogenic methane was likely generated at <80°C during early Late Triassic (Fig. 1B; Fig. S1). Oxidation of such biogenic methane by Mn oxides is most likely to follow Equation 1 or 2 to generate CO₂, resulting in a decrease in dryness coefficient (C₁/C_1–5) with increasing CO₂/(C_1–5 + CO₂) or CH₄ oxidation extents (Fig. 3C). This may have occurred in a closed environment with limited amounts of methane supply from all pools. This hypothesis is in line with the extremely ¹³C-depleted calcites with bulk δ¹³C values as low as −70‰ (Hu et al., 2018) and SIMS values as low as −58‰ in this study (Fig. 3B; Table S1). The calcite δ¹³C values are largely controlled by initial methane δ¹³C₁, carbon isotope fractionation, the oxidized methane–to–residual methane ratio, and the mixing proportion with inorganic CO₂ or HCO₃⁻ (Machel et al., 1995; Whiticar, 1999). The extremely ¹³C-depleted calcites (<−58‰) are expected to have resulted from the oxidation of ¹²C-enriched biogenic methane without significant contributions of inorganic CO₂ or HCO₃⁻. With increasing CH₄ oxidation degree as reflected in the CO₂/(C_1–5 + CO₂) ratio or MnO content, residual methane and thus newly generated calcite show progressively positive shifts in their δ¹³C values (Figs. 3B and 3D).

The sample Ma15 calcite is the product of CH₄ oxidation to the highest degree, as indicated by the highest average MnO content (7 wt%; Table S1), and shows the highest bulk δ¹³C value of −31‰ (Table 1). This suggests that the calcite may have carbon derived either from complete oxidation of residual methane, if both have similar δ¹³C values, or via mixing of carbon from oxidation of lighter methane with inorganic HCO₃⁻. The δ¹³C value of the pre-reacted methane to precipitate Ma15 calcite can be estimated from calcite Mn content and δ¹³C₁ relationship (Fig. 3B) to be heavier than −40.4‰. This is similar to the model for calculation of δ¹³C and δ⁵⁶Fe values of FeCO₃ from partial and near-complete microbial reduction of Fe(OH)₃ (Heimann et al., 2010). The oxidation may have occurred at <65 °C as shown from the clumped isotope data (Fig. 3A; Table 1). This is based on two aspects: (1) subsequent water-rock interactions do not significantly alter oxygen isotope fractionation in the calcites, thus Ma15 calcite has the most negative δ¹⁸O value and shows the lowest temperatures (Table 1), opposite of that expected from isotope re-equilibrium; and (2) the δ¹⁸O values of both sulfate and MnO₂ are lower than that of a calcite precipitated at oxygen isotope equilibrium with the diagenetic water; thus, clumped isotopes of the calcites from Mn-dependent AOM should record the maximum temperature, which is similar to a report for sulfate-dependent AOM (Loyd et al., 2016). Under such a low-temperature condition, only biogenic methane was charged into the reservoirs in the area, while oil and the associated thermogenic gas were not present until temperatures reached >85 °C (Fig. S1; Qi et al., 2015; Hu et al., 2018). Thus, biogenic methane must have been oxidized to form the calcites.

In contrast, three other calcites (Table 1) may have formed at <142 °C through TMnR by heavier hydrocarbons, rather than methane as previously proposed (Hu et al., 2018). This is because methane is not oxidized until most heavier alkanes are depleted, with C₁/C_1–5 > 0.95, as the result of methane as the most thermally stable compound among hydrocarbons (Machel, 2001; Cai et al., 2003, 2013). Calcite sample M154-3031.05 is of such a TMnR origin and thus has an isotopic temperature of 116 °C and contains oil fluid inclusions. This calcite shows higher δ¹³C value than the biogenic counterparts with similar MnO contents (Fig. 3B).

In summary, we present a case showing direct oxidation of biogenic methane by Mn oxides in a sulfate-poor freshwater lacustrine environment during early diagenesis at <65 °C prior to oil and thermogenetic gas charge, producing Mn-rich and ¹³C-depleted calcites. Such an origin of carbonates may have occurred in Mesoarchean carbonates (Ossa Ossa et al., 2018). Much more Mn-dependent AOM in Earth's history may have served as a significant sink of methane but has not yet been identified.

This study was financially supported by the National Natural Science Foundation of China (grants 41730424 and 4181101560). We thank Chad Wittkop and two anonymous reviewers for their constructive comments.