Anoxic Photogeochemical Oxidation of Manganese Carbonate Yields Manganese Oxide

Anoxic photogeochemical oxidation of manganese carbonate yields manganese oxide

Winnie Liua, Jihua Haob, Evert J. Elzingac, Piotr Piotrowiakd, Vikas Nandae, Nathan Yeea, and Paul G. Falkowskia,b,1

aDepartment of Earth and Planetary Sciences, Rutgers University, Piscataway, NJ 08854; bDepartment of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901; cDepartment of Earth and Environmental Sciences, Rutgers University–Newark, Newark, NJ 07102; dDepartment of Chemistry, Rutgers University–Newark, Newark, NJ 07102; and eDepartment of Biochemistry and Molecular Biology, Center for Advanced Biotechnology and Medicine, Rutgers University, Piscataway, NJ 08854

Contributed by Paul G. Falkowski, July 21, 2020 (sent for review February 7, 2020; reviewed by Kurt O. Konhauser and Timothy W. Lyons) The oxidation states of manganese minerals in the geological Mn and one Ca atom in a cubane structure that has no known record have been interpreted as proxies for the evolution of mineral analog (12). However, abiotic, sacrificial photochemical molecular oxygen in the Archean eon. Here we report that an reactions of manganese are known to have occurred (13–15). Archean manganese mineral, rhodochrosite (MnCO3), can be pho- Hence, an understanding of the photogeochemistry of manga- tochemically oxidized by light under anoxic, abiotic conditions. nese minerals may inform us about the transition from sacrificial Rhodochrosite has a calculated bandgap of about 5.4 eV, corre- to catalytic reactions of this transition metal and, thus, the bio- sponding to light energy centering around 230 nm. Light at that logical production of molecular oxygen on early Earth. Photo- wavelength would have been present on Earth’s surface in the geochemical reactions are sacrificial; that is, they are irreversible Archean, prior to the formation of stratospheric ozone. We show and consume the substrates (16). In contrast, biochemical reac- experimentally that the photooxidation of rhodochrosite in sus- tions are catalytic where the reactions are often reversible and pension with light centered at 230 nm produced H2 gas and man- the substrate is regenerated in a global cycle (17). Here we focus − ganite (γ-MnOOH) with an apparent quantum yield of 1.37 × 10 3 on photogeochemical reactions of manganese minerals. moles hydrogen per moles incident photons. Our results suggest While it is well known that photogeochemical reactions may that manganese oxides could have formed abiotically on the sur- have played a major role in early Earth biogeochemical cycles face in shallow waters and on continents during the Archean eon (13, 16, 18), it is not understood how these reactions could have in the absence of molecular oxygen. altered the surface oxidation state of Earth or how they could EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES have become appropriated and altered by life, to lead to pho- photogeochemistry | Archean manganese cycle | paleoredox proxies | tocatalytic reactions (14). All extant cyanobacteria contain two oxygen photosystems: one splits water to make hydrogen equivalents (i.e., electrons and protons), and the second uses the energy of terrestrial planet the size of Earth can only irreversibly lose light to push the electrons to more negative redox potentials Ahydrogen to space and thus, over geological time, become where they can be coupled to the protons to form a biological more oxidized (1). However, light can drive electron transfer carrier of reductant such as NAD(P)H (19). reactions far from thermodynamic equilibrium and oxidize a Here we focus on the photochemical reactions of manganese planet’s surface without hydrogen escape. Indeed, light is the minerals. We specifically examine the transition of Mn(II) to 0 − primary source of energy for the oxidation of molecules on Mn(III), which has a redox potential (E )of 1.54 V (20). This Earth’s surface, and the retention of hydrogen is the source of energy on Earth. How light interacts with surface minerals on Significance planets is very poorly understood. Here we discuss the potential for light to have abiotically oxidized early Earth. When oxygenic photosynthesis evolved is debated with an On Earth, the overwhelming source of hydrogen for life is uncertainty of approximately 1 Gy. It is generally assumed that water on the planet’s surface. The hydrogen (as protons and the oxidation of manganese minerals requires biological ca- electrons) is derived by the photobiological splitting of water by talysis or molecular oxygen and therefore is often used as a oxygenic photoautotrophs. How and when oxygenic photosyn- proxy for the presence of oxygenic photosynthetic organisms. thesis first arose is very poorly constrained (2–6). Geochemically, We show that anoxic, abiotic oxidation of the mineral rhodo- the upper bound of oxygenic photosynthesis is based on the chrosite (MnCO3) by UV light forms H2 and manganite discovery of a transition from mass-independent to mass- (γ-MnOOH). Our results reveal an alternative mechanism for dependent isotopic fractionations of sulfur (7). The mass- producing manganese oxides from rhodochrosite in the ab- independent fractionation is hypothesized to be driven by pho- sence of molecular oxygen. These results demonstrate the tochemical reactions between 195 and 215 nm (7, 8). The tran- potential impact of photogeochemical processes on the redox sition to a mass-dependent fractionation is inferred as a proxy for state of transition metals and hence question the interpreta- the evolution of stratospheric ozone at about 2.33 Ga (9, 10). tion of the rise of atmospheric oxygen based on the oxidation Our present knowledge of atmospheric geochemistry requires of transition metals, such as Cr isotopes. that molecular oxygen be a source of ozone. While the presence Author contributions: W.L., P.P., N.Y., and P.G.F. designed research; W.L. and E.J.E. per- of ozone does not constrain the lower boundary of O2, it requires formed research; P.P. and P.G.F. contributed new reagents/analytic tools; W.L., J.H., E.J.E, a source of the gas. On Earth, that source is oxygenic photo- V.N., N.Y., and P.G.F. analyzed data; and W.L., J.H., E.J.E., P.P., V.N., N.Y., and P.G.F. wrote synthesis, which evolved in the Precambrian, and is now the paper. expressed in one prokaryotic phylum: the cyanobacteria. Reviewers: K.O.K., University of Alberta; and T.W.L., University of California, Riverside. The formation of molecular oxygen by cyanobacteria required The authors declare no competing interest. several evolutionary innovations, and paleoproxies suggest that Published under the PNAS license. O2 may have arisen much earlier (3, 5, 11), before it could have 1To whom correspondence may be addressed. Email: [email protected]. significantly influenced the gas composition of Earth’s atmo- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ sphere. The core of the sole, extant, biological reaction center doi:10.1073/pnas.2002175117/-/DCSupplemental. that catalytically splits water and provides oxygen contains four

www.pnas.org/cgi/doi/10.1073/pnas.2002175117 PNAS Latest Articles | 1of7 Downloaded by guest on October 2, 2021 A 20 B H2 per mole incident photons. Using the Tauc method (30), the 18 bandgap value determined for rhodochrosite was 230 nm (SI 16 Appendix, Fig. S2). Irradiation of rhodochrosite suspensions with 14 0h 4h 8h 12h optical filters that transmitted light >250 nm did not produce H2. 12 The reactive wavelength was determined to be between 210 and

mol) 10 ( 250 nm, in agreement with the reactive wavelength range 2 8 H obtained from the bandgap analysis. Irradiation of MnCl2 with 6 the bandpass filter centered at 230 nm did not produce any de- 4 2 tectable H2 within 8 d, and no precipitate was formed matching 0 the observations of previous studies (15). 0 50 100 150 200 250 Time (hr) Mineral Product Characterization. Scanning electron microscope (SEM) analysis of the UV irradiated solids showed a difference Fig. 1. H production and formation of secondary material with reaction 2 in particle morphology between the reactant and product solids time. (A) The average production of H2 with reaction time for the 1.44 g/L μ reactions. The values plotted are the average of four replicates, and the (Fig. 2). The parent rhodochrosite was composed of 1 to 2 m error bars represent SE. (B) The change in suspension color with reaction diameter spherical globules aggregated in clusters (Fig. 2A). In time for the 1.44 g/L reactions. contrast, the secondary mineral product was more fine grained and fibrous (Fig. 2B). The unreacted globular particles in the irradiated sample were disaggregated and surrounded by the redox potential restricts the number of naturally occurring secondary mineral product. chemical oxidants that are capable of oxidizing Mn(II) (2, 21); The infrared spectrum of the irradiated sample exhibited the the most notable, geochemically relevant is molecular oxygen. rhodochrosite peaks as well as several new peaks at 594, 948, −1 Current biogeochemical models estimate Archean pO2 was at or 1,085, 1,120, 1,154, and 2,080 cm and a shoulder at around − below 0.001% of present atmospheric levels (22). Under such 630 cm 1 (Fig. 3). Of these new peaks in the irradiated rhodo- − − low concentrations, the redox cycling of manganese is generally chrosite spectrum, the 594 cm 1 peak and the 630 cm 1 shoulder thought to be limited (2) or potentially mediated by anoxygenic can be attributed to Mn–O lattice vibrations (31) while the peaks − photosynthetic bacteria (4, 23). Hence, the presence of manga- above 900 cm 1, particularly the group of peaks between 1,000 − nese oxide minerals is often inferred as a proxy of molecular and 1,200 cm 1, likely correspond to OH vibrations (32). These oxygen (2, 3, 5, 14). results suggest UV irradiation of rhodochrosite produces a Rhodochrosite (MnCO3) was a major Mn(II) mineral in the manganese oxyhydroxide phase containing both Mn–O and OH Archean (24–27). It has an optical bandgap between about 5.0 bonds. Comparison of the irradiated rhodochrosite IR spectrum and 5.8 eV (28, 29), indicating it can participate in photo- with the spectra of various Mn oxides and oxyhydroxides showed chemical reactions when excited with UV light at wavelengths that the manganite (γ-MnOOH) spectra matched the new peaks shorter than the absorption threshold in the 215 to 250 nm in the irradiated rhodochrosite spectrum, particularly those − window. The presence of rhodochrosite in Archean rocks (25) around 1,000 to 1,200 cm 1 and the Mn–O peak around − suggests it could have been exposed to UV light on the surface 590 cm 1. The spectrum of manganite is included in Fig. 3 for of continents through uplift of metamorphic and sedimentary reference. rocks by tectonic processes as well as possibly in the surface layer The Mn K-edge X-ray absorption spectroscopy (XAS) results of the water column. show that the spectrum of irradiated rhodochrosite (Fig. 4B, Here we investigate the photoreaction of rhodochrosite irra- blue) was dampened compared to the parent mineral and that diated by UV light under anoxic conditions. Our experimental the edge was shifted to slightly higher energy. These results in- data demonstrate that the photochemical redox transformation dicate changes in Mn bulk speciation that are difficult to assess of rhodochrosite by UV radiation leads to the formation of H2 because of the low content of irradiation product in the sample. and the manganese oxyhydroxide mineral manganite To better characterize the photooxidation product, the irradi- (γ-MnOOH). These experimental results suggest that mineral ated rhodochrosite was extracted with acetic acid to remove the photochemistry in the Archean manganese cycle provided an unreacted mineral and isolate the secondary product (Fig. 4A). alternative, abiotic pathway for the oxidation of manganese The edge energy of the secondary mineral product was higher minerals and their proxies. than that of the parent rhodochrosite material (Fig. 4B). This Results Photoreactivity and Headspace Analysis. Gas chromatography analysis of the headspace after UV irradiation of suspensions of rhodochrosite revealed that H2 was produced (Fig. 1A). The production of gaseous H2 was concurrent with the formation of a dark colored secondary mineral in the solid phase (Fig. 1B). The 1.44 g/L rhodochrosite suspensions produced 18.0 μmol H2 while the 0.57 g/L suspensions produced 14.6 μmol H2. The reaction was associated with acidification (SI Appendix, Fig. S1). Se- quential extraction of the product showed a decrease in the carbonate fraction and an increase in the dissolved and oxide fractions with reaction time (SI Appendix, Fig. S1). In control experiments, H2 production and secondary mineral formation did not occur in the absence of UV light. No organic acid production was detected. Fig. 2. SEM images before and after irradiation. (A) The reactant rhodo- Apparent Quantum Yield. The apparent quantum yield at 230 nm chrosite before irradiation. (B) The irradiated rhodochrosite. The magnifi- −3 for the photooxidation of rhodochrosite was 1.37 × 10 moles cation was 12,500× for both images. (Scale bar, 5 μm.)

2of7 | www.pnas.org/cgi/doi/10.1073/pnas.2002175117 Liu et al. Downloaded by guest on October 2, 2021 A proposed overall balanced reaction is

0.30 hv II III − + 2Mn CO3 + 4H2O→2γ − Mn OOH + H2+2HCO + 2H , Manganite 3 0.25 [1]

0.20 where manganite and hydrogen gas are formed from rhodochro- * site and water in a two-electron reaction driven by UV light. The * + 0.15 Irradiated rhodochrosite * * production of H results in a decrease in pH as the reaction SI Appendix Absorbance * * proceeds ( , Fig. S1). Although not experimentally 0.10 determined directly, the carbonate from the rhodochrosite either remains in the solution or forms CO2 after oxidation. Based on − 0.05 the pH throughout the reaction, HCO3 is likely the dominant product species. This mechanism would uphold in Archean wa- Rhodochrosite − 0.00 ters. The addition of HCO3 would buffer the decrease in pH. 2500 2000 1500 1000 Using thermodynamic data for rhodochrosite and manganite, the Δ o -1 Grxn of the overall reaction is 297 kJ/mol (33, 34). The reac- Wavenumber (cm ) tion is therefore endothermic, and under anoxic conditions, en- Fig. 3. IR spectra for the irradiated and reactant rhodochrosite. New peaks ergy from light or heat is required. The wavelength of light used in the irradiated rhodochrosite spectra are labeled with asterisks. The to induce the reaction was ∼230 nm, corresponding to 520 kJ/ spectrum of manganite is shown in brown on top for reference. mol, giving an excess energy of 223 kJ/mol (i.e., 2.3 V). Discussion indicates a change in manganese oxidation state, as demon- The results of this study reveal that the abiotic photooxidation of strated by the XAS spectra of the standards showing that the Mn rhodochrosite under anoxic conditions results in the production K-edge position shifts to higher energies with increasing Mn of manganite and H2 gas. This process can be driven entirely by valence. The Mn K-edge position of the secondary mineral light at Earth’s surface temperatures and does not require the product best matched that of a MnOOH reference consistent presence of a chemical oxidant or a biological reaction. The 2+ 3+ production of an Mn(III) mineral from a Mn(II) mineral with a change in oxidation state from Mn to Mn . EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES X-ray diffraction analysis of the acetate-extracted mineral (Fig. 4B) demonstrates that direct photochemical reactions of product showed peaks at d spacings of 3.405, 2.640, 2.415, and manganese minerals are a possible mechanism for oxidizing 1.672, corresponding to 2θ peaks at 26.17°, 33.96°, 37.23°, and manganese. While these reactions could also occur biologically 54.91°, respectively (Fig. 5). The X-ray diffractogram of the (4, 23), our data suggest a simple process that could occur in the secondary mineral matched that of manganite (γ-MnOOH), in presence of UV radiation. The production of H2 plateaued over agreement with the IR analysis. The irradiated rhodochrosite time (Fig. 1A) suggesting that UV photooxidation can only that did not undergo extraction with acetic acid retained the partially oxidize the manganese, and the photoreaction is limited rhodochrosite peaks as well as exhibited new peaks at d spacings by the surface area exposed to photons and water. Even on of 3.403, 2.640, 2.522, and 1.671, corresponding to 2θ peaks at geological time scales, this is a factor potentially limiting full 26.17°, 33.96°, 35.60°, and 54.95°. These new peaks also matched oxidation of the mineral before the evolution of molecular oxy- the major manganite peaks. The irradiated sample was therefore gen in Earth’s atmosphere. a mixture of rhodochrosite, the reactant, and manganite, the How rhodochrosite could have been formed in the Archean is product, in agreement with the results of the SEM and IR critical to the interpretation of the relevance of the photo- analyses. The presence of manganite in both the extracted and chemical reaction with respect to proxies for the evolution of unextracted product indicates that the acid extraction did not molecular oxygen. In modern settings, rhodochrosite is primarily change the mineralogy of the product. formed in the sediments from the reaction of manganese oxides

3 A B Extracted Irradiated rhodochrosite e nc

a 2 b r o Irradiated rhodochrosite

Normalized Abs 2+ Mn CO3 Mn3+OOH 4+ 0 Mn birnessite 6.53 6.54 6.55 6.56 6.57 6.58 6.59 6.60 Energy (keV)

Fig. 4. SEM image and XAS spectra for the extracted irradiated rhodochrosite. (A) SEM image for the extracted irradiated rhodochrosite at 12,500× magnification. (Scale bar, 5 μm.) (B) XAS spectra for the extracted irradiated rhodochrosite (green) and irradiated rhodochrosite (blue). Samples with known Mn2+,Mn3+, and Mn4+ oxidation states are shown underneath with vertical lines at the halfway edge energy. The halfway edge energies were 6.553, 6.558, and 6.562 for Mn2+,Mn3+, and Mn4+, respectively. The Mn2+ standard was the parent material rhodochrosite, while the Mn3+ and Mn4+ standards were MnOOH and Mn(IV) birnessite, respectively.

Liu et al. PNAS Latest Articles | 3of7 Downloaded by guest on October 2, 2021 130 Mn-silicate, which often cooccurs with rhodochrosite in meta- 120 Manganite morphosed sediments (50, 51). Therefore, as indicated by our 110 compilation (SI Appendix, Tables S1 and S2), rhodochrosite 100 Extracted precipitation might have been feasible in Archean seawater or 90 Irradiated Rhodochrosite pore water or during cooling of hydrothermal fluid and thus at 80 least locally available for photoreaction. Nevertheless, after 70 Irradiated Rhodochrosite burial in marine sediments, manganoan carbonate in marine ensity t 60 * * * * sediments would have been uplifted and exposed to sunlight In 50 following the exposure of the continental land in the mid- 40 Archean (52, 53). In addition, the precipitation of Mn-rich car- 30 bonates in soil systems is thermodynamically favorable under the 20 high-pCO2 conditions of the Archean (41). Although the pene- 10 Rhodochrosite tration depth of UV light in soil and particulate minerals is much 0 shallower, ranging from 10 μm to 1 mm (54–56), in continental 20 25 30 35 40 45 50 55 60 65 70 75 80 settings this process would not require the mineral to precipitate °2θ (Cu Kα) and stay suspended within the photic zone for extended periods Fig. 5. XRD results for the extracted irradiated, irradiated, and reactant of time. rhodochrosite. The new peaks in the irradiated rhodochrosite spectrum are Regardless of how rhodochrosite formed, our results have labeled with an asterisk. The spectrum of manganite is shown in brown on significant geochemical implications for the interpretation of the top for reference. geological record in deep time. Manganite is the most stable Mn(III) hydroxide and plays a role in carbon and metal cycling (57, 58). It is also an important natural oxidizing agent and has with organic matter, and the role of organic matter is evident in been shown to oxidize organic acids like oxalic acid and glyoxylic the negative carbonate δ13C values (27). While few studies have acid (59). The lack of organic acid production in the irradiation measured the δ13C of Archean rhodochrosite prior to 2.6 Ga experiments is therefore unsurprising since even if the photore- (26), the negative δ13C values, between −22.3 and −13.5‰ action produced organic compounds, either the manganite or the Vienna Pee Dee Belemnite (VPDB), of Mn-Fe–rich carbonates UV light would have degraded them. Manganite also affects the in the Mesoarchean Mozaan Group, Panogola Supergroup, biogeochemical cycling of trace metals through adsorption and/ South Africa (ca. 2.98 to 2.85 Ga), support this mechanism (35). or oxidation reactions, for example, Zn adsorption (60), As ox- Another noncompetitive possibility is the formation of man- idation (61), Cr oxidation (5, 62), and Fe oxidation (21). The ganoan carbonates in the anoxic water column (36, 37). Studies photooxidation of rhodochrosite may have been an important in modern-day redox stratified lakes, for example, show it is manganese recycling mechanism to help retain a biogeochemi- possible to form manganese-rich carbonates where calcite pro- cally important oxidant. vides nucleation sites for manganoan carbonate precipitation in Because manganite is also chemically reactive, it would likely the water column (36, 37). The isotopic signature of these car- back-react in the dark with reducing minerals, dissolved species bonates is higher, around –4.3‰, indicating less contribution in soil waters, and reducing gases. Indeed, Postma and Appelo from organic matter (38). Alternatively, calcite dissolution below (63) showed that reduction of manganite by sulfide and ferrous a shallow lysocline could supply additional carbonate and also iron could reach completion within 10 h under ambient condi- result in manganoan carbonate precipitation in reducing, high- tions. Johnson et al. (64) showed rapid reduction of MnOx by manganese environments (39). sulfide and ferrous iron also within 10 h. In addition, microor- A similar process could have occurred in the Archean to form ganisms can also facilitate reduction of MnOx using organic manganoan carbonates in the photic zone of shallow seas. matter. This is a major process of the Mn cycle in modern sea- During the Archean, the concentration of manganese was higher water. Reduction of manganite and/or other manganese oxides 2+ due to the high solubility of Mn(II) with estimates in the mi- would have generated either dissolved Mn or MnCO3 when cromolar region (2, 40, 41). These values are similar to the values carbonate species are available which would hamper the long- in the modern lake mentioned above (∼1 μM) (37). Further- term preservation of manganite until the reductants were −2.5 more, pCO2 was almost certainly much higher, ≥10 atm exhausted or oxidized. However, in the short term, the photo- − compared to present-day ∼10 3.5 atm, with correspondingly reaction could deliver a supply of strong oxidant to early higher dissolved inorganic carbon (DIC) estimates (42, 43). biogeochemical environments. Rhodochrosite is fairly insoluble (–log Kso = 11.65) (44); thus, Manganite is also known to disproportionate into MnO2 and formation of the mineral could have been thermodynamically Mn2+ under acidic conditions through the following reaction: favorable in Archean waters under higher DIC and circum- SI Appendix + 2+ neutral pH conditions ( , Fig. S7). If precipitation of 2γ − MnOOH(s) + 2H ⇋MnO2(s) + Mn + 2H2O(58). [2] manganoan carbonates occurred within the photic zone, up to 80 m in nonturbid waters, in either seawater or lake water during Assuming manganite is preserved long enough under geochem- the Archean, it would have been available for photooxidation (45). ical conditions favorable to disproportionation, the photooxida- Archean rhodochrosite also could have also formed through tion of rhodochrosite and the subsequent disproportionation to hydrothermal and soil processes. Mixing of Mn-rich hydrother- Mn(IV) oxides provides a plausible mechanism for the formation mal fluids (2.25 mM in modern hydrothermal fluid altering ul- of higher valent manganese oxides with only UV light. Mn(IV) tramafic rocks) (46) with carbonate-rich Archean seawater oxides are also reactive toward organic acids (59) and can adsorb would be expected to precipitate rhodochrosite. Indeed, rhodo- or incorporate a range of metals including Cr, Mo, Fe, Co, Ni, chrosite is a major manganese mineral in hydrothermal manga- Cu, Zn, Cd, Pb, etc. (57). Overall, the manganite produced by nese deposits (e.g., ref. 47), and Archean manganese-rich rocks UV radiation of manganoan carbonates likely would have been show a strong signal of hydrothermal input (48, 49). It is worth short-lived in the Archean because of reactions with reductants mentioning that Archean sedimentary rocks have experienced at like sulfides and ferrous iron. This short lifetime is unlikely to least low-grade metamorphism which may undermine the pres- support riverine transport of manganite or manganese oxide par- ervation of rhodochrosite via decarbonation to form MnO or ticulates, which is in the time scale of thousands of years (65, 66),

4of7 | www.pnas.org/cgi/doi/10.1073/pnas.2002175117 Liu et al. Downloaded by guest on October 2, 2021 or deposition into marine sediments (67). Therefore, despite between the spectrum of light reaching the sample and the ab- possible photooxidation of rhodochrosite and production of sorbance of dissolved Mn. This small absorption cross-section manganite on Archean continents, it is unlikely to have supplied indicates that dissolved Mn is unlikely to be responsible for the substantial amounts of oxidized manganese to early ocean(s) or reaction. In addition, the concentration of dissolved Mn in- to have supported the creation of large manganese ore deposits creased as the rhodochrosite was irradiated, suggesting it is more until the reductants were exhausted. likely a product than a reactant (SI Appendix, Fig. S1). Does the redox state of manganese minerals establish the time In addition to rhodochrosite photooxidation, dissolved Mn(II) of the evolution of oxygenic photosynthesis? Several other can be directly photooxidized to birnessite by UV light (13) or − paleoredox proxies, such as Cr isotopes, have invoked manga- indirectly by NO3 photolysis (15), but dissolved Fe(II) interferes nese oxides to link the proxy itself to the presence of molecular with the former reaction while the latter reaction requires the oxygen (3, 5). In the case of Cr isotopes, the oxidative dissolution presence of nitrate, which was a very unstable ion in the Archean of Cr(III) in continental rocks to more soluble Cr(VI) usually (79). According to our calculations, Mn(II) in minerals of sur- requires strong oxidants such as Mn oxyhydroxides or hydrogen ficial sediments would have much higher abundance than dis- peroxide due to slow kinetics (68, 69). Manganite, the photore- solved species in Archean surface seawater indicating a action product, is capable of oxidizing Cr(III). For example, potentially more important role of manganese mineral photo- Johnson and Xyla (62) reported that at pH = 4.5, oxidation of chemistry than for aqueous processes (see SI Appendix, SI Ma- Cr(III) by manganite could reach completion within an hour. terial, for further discussion). Dissolved Fe(II) could potentially This pH is close to that of Archean weathering fluid at Archean also interfere with the photooxidation of rhodochrosite; how- pCO2 (41). Their experiments showed that oxidation of Cr(III) ever, the absorption spectrum of FeCl2 overlaps that of MnCl2 by manganite is 10 to 10,000 times faster than for other Mn more than rhodochrosite (see SI Appendix, SI Material, for fur- oxides, implying that manganite is an efficient oxidant for ther discussion). In addition, on land, Archean rainwater would Cr(III). The manganite generated via photooxidation of rhodo- contain less dissolved Fe(II), implying much less interference chrosite is likely smaller in size than the large crystals used in the with photooxidation of rhodochrosite in surface sediments. Johnson and Xyla experiment (62). Therefore, the oxidation rate Atmospheric absorption of solar radiation, especially from of Cr(III) by the photogenerated manganite could be even faster. CO2 and H2O, restricts the surface of Earth to radiation above The oxidation of Cr(III) by manganite in Archean soil results in 200 nm (80). Solar analog spectral radiance data for an early Sun the mobilization and transport of Cr(VI) to the ocean and an show that the irradiance around 230 nm was higher than that isotopically heavy Cr(VI) pool (62, 69). Indeed, Joshi (70) ob- between 200 and 210 nm (81). This higher photon flux would ‰ served a positive Cr isotopic fractionation up to 0.65 during have increased the photooxidation of rhodochrosite. Further- EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES oxidation of Cr(III) by manganite. After riverine transport, the more, because rhodochrosite is a solid, the photoreaction can isotopically heavier Cr(VI) could have been back reduced by occur in soil or shallow sediments of continental waters, there- reductants and preserved in marine sediments (5, 71–73). fore expanding the possible environments where the reaction Overall, our experimental results offer an alternative interpre- could have occurred. This is critical as Cr(III) oxidation by Mn tation for small positive anomalies of Cr isotopes in ancient oxyhydroxides primarily occurs on land within soils (82). sedimentary rocks. Rhodochrosite was one of the major Archean manganese Molecular H2 was the reduced product identified in the pho- minerals (2, 24) and was exposed to UV light in that eon. Our tochemical reaction and is an important biogeochemical reduc- results suggest that an alternative mechanism for producing tant. H2 is used in microbial metabolism by prokaryotes; a local manganese oxides from rhodochrosite in the absence of molec- source of H2 could have helped sustain early lithotrophic mi- ular oxygen was abiotic photooxidation. This photoreaction oc- crobial communities (74). The photochemical oxidation of min- curs at higher wavelengths than the previously studied dissolved erals was potentially a significant source of H2 in Archean Mn(II) photoreaction suggesting that there was potentially more shallow waters. Rhodochrosite, as well as other minerals, in- anoxic manganese oxide production than previously considered cluding siderite (FeCO3) and Fe(OH)2 all produce H2 when (2, 83). Manganite, the product of the photoreaction, is capable photooxidized (75, 76). Kim et al. (75) estimated global H2 of oxidizing both organic compounds and metals and, as such, production from the photooxidation of siderite to be ∼2 × 1010 plays a role in geochemical cycling of many elements. This could mol H2/y. The production and the eventual escape of H2 to space have important implications for paleoredox proxies such as the can lead to the oxidation of the planet over time (1). H2 is also a oxidative weathering of chromium and fractionation of chro- potential greenhouse gas (77). The apparent quantum yield mium isotopes. The photoreaction with rhodochrosite could measured in this study for rhodochrosite is similar to that of have delivered a supply of strong oxidant to early environments. siderite (75). However, the abundance of rhodochrosite in the This reaction demonstrates the potential role of mineral pho- Archean was likely significantly less than that of siderite given tochemistry in Archean biogeochemical cycling. Further work in their similar geochemical properties and relative abundances in studying these reactions in more complex systems is needed to the upper continental crust (78). Thus, the photooxidation of better characterize their impact in the Archean, for example, the rhodochrosite would have contributed more as a supplementary photoreactivity of mixed calcium manganese carbonates (e.g., source globally or as a local source of H2 in areas with high kutnahorite) which often form instead of pure rhodochrosite as manganese. well as the potential interaction with iron both in dissolved form The lack of H2 production and precipitate formation in the and as a mix with siderite. Despite the lack of understanding water and MnCl2(aq) control experiments at 230 nm confirms regarding the photoreactivity of carbonate solid solution systems, that rhodochrosite is the photoreactive species. The bandpass we emphasize that photooxidation of rhodochrosite, as a pure filter used to experimentally determine this only transmits light end member phase, would have still been important in regions between 210 and 270 nm which matches the wavelengths of light enriched in manganese. absorbed by rhodochrosite (SI Appendix, Fig. S4). The MnCl2 Finally, we note that in the evolution of the photobiological control did not show any reaction when irradiated with UV light oxidation of water, the catalytic site of the extant catalytic re- passing through the 228FS25 bandpass filter indicating that the action center, the oxygen evolving complex of photosystem II, energy required to directly photooxidize dissolved Mn(II) is contains four Mn atoms, two of which undergo four sequential higher than 5.9 eV (<210 nm). Indeed, dissolved Mn(II), with one photon, one electron transfers (84). The four Mn atoms are and without carbonate present, shows almost no absorbance coordinated with one Ca ion through oxo bridges. The origin of above 210 nm (SI Appendix, Fig. S5). There is little overlap this biological mineral in oxygen evolving complexes in photosystem

Liu et al. PNAS Latest Articles | 5of7 Downloaded by guest on October 2, 2021 II reaction centers remains ambiguous; however, the resultant prod- Apparent Quantum Yield. The Andover Corp. 228FS25 bandpass filter with a ucts are electrons and protons (i.e., hydrogen equivalents but not central wavelength of 230 nm was used to determine the apparent quantum hydrogen gas) and oxygen. A key issue in the evolution of this yield of H2. A 1.78 g/L suspension of rhodochrosite was irradiated for 8 d, and globally transformational reaction is how sacrificial photo- the H2 production per d was determined. Two control samples, one with geochemical reactions of manganese minerals became catalytic deoxygenated water only, the other with 0.5 mM MnCl2, were also irradi- photobiological reactions. ated for 8 d under the same conditions. The 0.5 mM MnCl2 concentration is much higher (>100×) than the concentration of dissolved Mn present in a Materials and Methods 1.78 g/L rhodochrosite suspension. The absorbance spectra of the MnCl2 solutions with and without carbonate were obtained using an Agilent Cary Rhodochrosite Synthesis. Rhodochrosite was synthesized in an anaerobic 60 UV-Vis spectrophotometer. The apparent quantum yield (ξ) for the pro- chamber (Coy Laboratory Products) by mixing solutions of MnCl2 (250 mL, duction of H2 was calculated using the equation ξ = νp/Io where νp is the 0.25 M) and Na2CO3 (125 mL, 0.6 M) while stirring. The white precipitate formed was washed with deoxygenated MilliQ water multiple times to moles of H2 produced per unit time and the Io is the moles of incident remove excess ions and decrease the pH. The precipitate was analyzed with photons per unit time (85). The incident photon flux was determined using a XRD to confirm the synthesis of the mineral. The surface area of the syn- ferrioxalate actinometer (86), and the photon flux density through the 2 μ 2 thesized rhodochrosite was ∼19.5 m /g as measured by Brunauer–Emmett– 228FS25 bandpass filter was 0.48 mol quanta/m /s. Teller (BET) analysis. Diffuse reflectance UV-Vis spectroscopy was used to calculate the bandgap using the Tauc method (SI Appendix, Fig. S2) (85). Solid Analysis. The 0.57 g/L irradiated product was centrifuged at 6,000 × g for 10 min. The supernatant was removed, and the solid was dried in the an- UV Irradiation. The rhodochrosite suspension was diluted with deoxygenated aerobic chamber. The irradiated solid product was analyzed by SEM, IR, XAS, MilliQ water to the target concentration (1.44 or 0.57 g/L) in an anaerobic and XRD. chamber; 20-mL subsamples of this diluted suspension were transferred to To better characterize and identify the irradiation product, acetic acid quartz reaction cells and purged with N2 gas. These concentrations were (0.7 M HOAc at pH 4) was used to remove the unreacted rhodochrosite in the chosen in order to optimize analysis of the products. The reaction cells are 1.44 g/L suspensions that had been irradiated for 11 d. The remaining product composed of quartz at the bottom and fitted to use gas impermeable butyl was centrifuged at 6,000 × g for 10 min, washed four times with deoxy- rubber stoppers and aluminum crimp seals. This design prevents gas ex- genated MilliQ water, and then dried in the anaerobic chamber. The change with the atmosphere during the irradiation while allowing UV light extracted irradiated product was analyzed by SEM, XAS, and XRD to char- penetration to the sample. A 450-W Hg vapor lamp (Hanovia PC451.050) in a acterize the morphology, oxidation state, and mineralogy of the product. photochemical quartz immersion well was used to irradiate the samples. The detection of manganite in the unextracted irradiated samples indicates Magnetic stirrers were used to keep the mineral in suspension during the that the acetic acid from the extraction procedure did not react with or irradiation. The 0.57 g/L rhodochrosite suspensions were irradiated ∼5d change the secondary mineral product. while the 1.44 g/L suspensions were irradiated ∼11 d. The dark controls were

placed in N2 purged serum bottles wrapped in aluminum foil and stirred Data Availability. All study data are included in the article and SI Appendix. with a magnetic stirrer. UV bandpass filters (Andover 228FS25 centered around 230 nm, Semrock FF01-260/16 centered around 260 nm, and Asahi Spectra XHQA-270 centered around 270 nm [SI Appendix, Fig. S6]) were used ACKNOWLEDGMENTS. We thank Kevin Wyman, Shun Yu, Ashley Pennington, to determine the photoreactivity at specific wavelength ranges. and Kaixuan Bu for their help with data analysis and collection; Piotr Nawrot and Maxim Gorbunov for their assistance in constructing the photochemical apparatus; and Dr. Jeffrey Post at the Smithsonian Museum for comments on Headspace and Solution Analysis. The production of H2 was measured by gas the results of the study. We also like to acknowledge Argonne National chromatography with a thermal conductivity detector (Model 310, SRI In- Laboratory for use of the Advanced Photon Source, a US Department of struments). HPLC (Bio-Rad Animex HPX-87H) was used to check for the Energy (DOE) Office of Science User Facility operated for the DOE office of production of organic acids, and a pH probe was used to measure the pH of Science by Argonne National Laboratory under contract DE-AC02-06CH11357, the 1.44 g/L irradiation for the first 12 h. The manganese speciation was and we thank the beamline scientists at 12-BMB for assistance with XAS data determined using a sequential extraction procedure described in SI collection. This research was supported by NASA Exobiology Grant NNX16AK02G Appendix, SI Materials. and NASA Astrobiology Institute Grant 80NSSC18M0093.

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