Abstract
Biogenic magnetite is a potential biosignature for microbial iron cycling in hydrothermal sulfide systems, critical environments for unraveling the emergence and early evolution of life. However, the preservation potential of biogenic magnetite under hydrothermal conditions is poorly understood. Here, we show that the hydrothermal sulfidation of abiogenic and biogenic magnetite (sulfide/iron = 4, 80 °C) yields pyrite with various distinct morphologies, including framboid-like spheroids. We demonstrate that the variability in pyrite morphologies resulted from the modulation of pyritization rates by interrelated effects between organic matter and elemental sulfur (crystalline or colloidal). Notably, framboid-like pyrite, commonly considered a potential fingerprint of microbial sulfur cycling, was exclusively produced from the hydrothermal sulfidation of biogenic (i.e., organic matter-associated) magnetite produced by iron-cycling microorganisms. Thus, framboid-like pyrite can additionally be a taphonomic fingerprint of microbial iron cycling, enabling a better understanding of the evolution of Earth’s biosphere in deep time.
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Introduction
Hydrothermal systems are prime environmental candidates for life’s emergence due to their potential role in prebiotic organic synthesis1,2,3, their steep physical and chemical gradients establishing disequilibrium conditions4,5, and their existence on Earth for at least 3.77 billion years2,6,7,8,9,10. Hydrothermal systems potentially occurred in past surface environments on early Mars11 and in modern subsurface oceans of Enceladus12, underscoring their astrobiological significance. Therefore, understanding the proliferation of a microbial biosphere under hydrothermal conditions is crucial. This task requires tools for unraveling the interactions of minerals, organic compounds, and microorganisms in hydrothermal systems on the early Earth. Microbial biosignatures in early Earth’s rock record are our only archive for investigating these interactions in deep time10. Thus, better constraining the formation and preservation of microbial biosignatures in ancient hydrothermal deposits is fundamental for understanding the emergence and subsequent evolution of life on our planet and beyond.
Nano-magnetite [Fe3O4] is an essential piece in this puzzle due to its ubiquitous bio-mediated formation in early Earth’s oceans and its potential role in catalyzing vital prebiotic chemical reactions in hydrothermal systems1,13,14. On modern Earth, nano-magnetite forms by abiotic Fe(II)-driven transformation of Fe(III) (oxyhydr)oxides or via iron-cycling microorganisms, such as dissimilatory Fe(III)-reducing prokaryotes or magnetotactic bacteria15,16,17. Dissimilatory Fe(III)-reducing prokaryotes and magnetotactic bacteria are thought to have emerged in the Archean18,19, and commonly occur in modern hydrothermal sulfide environments20,21,22,23. Indeed, strain 121 (Geogemma barossii), one of the most heat-tolerant microorganisms known on Earth to date, is a magnetite-producing Fe(III)-reducing archaeon isolated from a black smoker system24, highlighting the role of magnetite biomineralization under hydrothermal conditions. Biogenic magnetite has specific morphologic, crystallographic, magnetic, and geochemical properties that differ from abiogenic magnetite15,25,26,27,28,29,30,31. Biogenic magnetite is also closely associated with organic matter, namely the cells and extracellular polymeric substances of microorganisms involved in its formation28,30. These properties make biogenic magnetite a potential biosignature of iron-cycling microorganisms in hydrothermal environments.
In hydrothermal environments, magnetite might be affected by sulfide delivered from hot and acidic fluids (up to ~400 °C; pH 2–5)32 and microbial sulfur cycling33, likely exerting a dominant control on its preservation34. This is because sulfide can drive the rapid reductive dissolution of nano-magnetite34,35,36,37,38,39,40. Magnetite sulfidation leads to the formation of secondary iron sulfides, including mackinawite [FeSm], greigite [Fe3S4], and pyrite [FeS2]34,35,39. The mechanisms and rates of these reactions, and the potential transformation of secondary iron sulfides to pyrite, are affected by temperature, solution Eh and pH, sulfur/iron ratio, magnetite stoichiometry, and the presence of trace metal(loid)s34,39,40,41,42,43,44,45,46,47,48. Moreover, elemental sulfur [S0], a ubiquitous intermediate sulfur species in hydrothermal systems, can strongly affect magnetite pyritization rates and pyrite morphology34. This implies that diagenetic processes in hydrothermal sulfide systems substantially alter biosignatures associated with magnetite.
Previous studies have not considered the interrelated effects of sulfur species (i.e., sulfide, S0, polysulfides) with organic matter (e.g., microbial biomass) that would be present during the hydrothermal sulfidation of biogenic magnetite. Organic matter is known to affect the surface reactivity and aggregation behavior of Fe(III) (oxyhydr)oxides, including magnetite, and secondary iron (mono)sulfides47,49,50,51,52,53. This potentially influences the textural and geochemical characteristics of the resulting pyrite, which commonly serves as a biosignature of sulfur-cycling microorganisms. For instance, pyrite exhibiting a framboidal morphology is widely used to track microbial sulfur cycling, especially if it encodes 34S-depleted sulfur stable isotope signatures (δ34Ssource - δ34Spyrite > 20‰)54,55,56,57. Framboidal pyrite from modern and ancient environments is commonly associated with organic matter, suggesting an essential role of organic templates in its formation55,56. However, experimental work on pyrite formation in active sulfur- and iron-cycling microbial cultures, as well as abiotic diagenesis of biogenic FeS (i.e., in the presence of microbial biomass but no living cells) at high temperatures (75–150 °C), yielded <1–5 µm-sized pyrite spheroids that do not show the typical raspberry-like texture commonly seen in framboids58,59,60,61. Furthermore, some experimental studies without organic matter demonstrated abiotic formation pathways for framboidal pyrite (see review by ref. 62). Nevertheless, while the direct role of microorganisms influencing framboid formation is elusive, organic matter appears to have a strong impact on pyrite morphology in natural environments. However, the identity and morphology of iron sulfides from the sulfidation of biogenic magnetite under hydrothermal conditions have not been constrained.
Here, we demonstrate experimentally that abiogenic and biogenic magnetite sulfidation under sulfidic hydrothermal conditions (60 mM sulfide, 15 mM iron, in anoxic artificial seawater at 80 °C, pH 7.5) yields various pyrite morphologies, including framboid-like spheroids. With µ-X-ray diffraction (µ-XRD), Raman spectroscopy, geochemical analysis (Fe(II)aq and sequential iron extraction), ultraviolet-visible (UV-Vis) spectroscopy, and scanning electron microscopy (SEM) supported by focused-ion-beam (FIB) milling, we show that the interrelated effects of organic matter and S0 (62 mM) on magnetite sulfidation rates and mechanisms control the variability of pyrite morphotypes. Notably, our study demonstrates that framboid-like pyrite results from the hydrothermal sulfidation of biogenic magnetite but not abiogenic magnetite. Thus, framboid-like pyrite may not only fingerprint microbial sulfur cycling but also record microbial iron cycling in hydrothermal sulfide systems.
Results
Mineralogical analyses
After 7 days of incubation, magnetite was neither detected by µ-XRD nor by Raman spectroscopy in any experimental setup (Figs. 1 and 2). Instead, pyrite formed in all experiments as indicated by characteristic Raman bands at 330–333 cm−1 and 366–371 cm−1 (Fig. 2). Pyrite is absent from µ-XRD patterns in experiments with abiogenic magnetite crystalline S0 (Fig. 1). Also, pyrite was not detected by µ-XRD in any experiment with biogenic magnetite (Fig. 1). This could be due to a pyrite content below the limit of detection or a poor degree of crystallinity. Mineral products from experiments with abiogenic magnetite also showed Raman bands characteristic of Fe(III)-containing mackinawite (Fe(III)-FeSm: 310–319 cm−1)63, but only in the absence of S0 (Fig. 2). In contrast, all experiments with biogenic magnetite contained Fe(III)-FeSm (Fig. 2).
Mk: Mackinawite; Py: Pyrite; S: S0. Please note that one sample from the experiment with abiogenic magnetite and colloidal S0 (35 days) could not be analyzed due to technical problems with the instrument.
Mk: Fe(III)-FeSm, Py: Pyrite. Note that Fe(III)-FeSm was detected in experiments with biogenic magnetite and S0 after 7 days but not in experiments with abiogenic magnetite.
After 21 days of incubation, the mineralogical composition of experiments with abiogenic magnetite remained unchanged (Figs. 1, and 2). The appearance of µ-XRD reflections characteristic for pyrite in experiments with both abiogenic and biogenic magnetite (+S0) may reflect an increasing degree of crystallinity (Fig. 1). In experiments with biogenic magnetite and S0, Fe(III)-FeSm was no longer detected using Raman spectroscopy (Fig. 2). In contrast, µ-XRD reflections characteristic of FeSm are still present (Fig. 1). This is most likely due to the limited spot size during in-situ analysis by Raman spectroscopy.
After 35 days of incubation, pyrite was detected in experiments with biogenic magnetite (no S0) using µ-XRD (Fig. 1). Overall, µ-XRD reflections characteristic of pyrite are broader in the presence of S0 (Fig. 1), indicating greater variability in d-spacing consistent with a lower degree of crystallinity.
Geochemical analysis
In experiments with and without crystalline S0, Fe(II)aq was between 43–74 µM at t0 and decreased to <10 µM during the experiment (Fig. 3a, Supplementary Data 1). Much higher Fe(II)aq concentrations occurred in the presence of colloidal S0 (304 µM and 105 µM with abiogenic and biogenic magnetite, respectively; Fig. 3a). After 3 days of incubation, Fe(II)aq concentrations in experiments with colloidal S0 were in the range of the other experiments (Fig. 3a).
The error bars represent the standard deviations of a minimum of experimental duplicates. a Aqueous phase (Fe(II)aq: combined dissolved and colloidal iron); b Degree of pyritization (DOP) as determined via sequential iron extraction of the solid phase using 6 M HCl (magnetite/FeSm/greigite) and 8 M HNO3 (pyrite).
Sequential iron extraction on the solid phase indicated a much faster increase in the degree of pyritization [Fe(HNO3)/[Fe(HCl)+Fe(HNO3)]] in the presence of S0 for both abiogenic and biogenic magnetite (Fig. 3b, Table 1, Supplementary Data 1). Pyritization proceeded faster in experiments with colloidal S0 than with crystalline S0 for both abiogenic and biogenic magnetite (Fig. 3b, Table 1). Regardless of the presence of S0, pyritization rates were slower with biogenic magnetite (Fig. 3b, Table 1).
Ultraviolet-visible (UV-Vis) spectroscopy
At the start (t0), experiments with colloidal S0 showed increased UV-Vis absorbances across the analyzed spectrum (250–500 nm) compared to all other experiments (Fig. 4a). This is likely due to the presence of colloidal FeS in the supernatant. After 3 days, a yellow coloration of the supernatant indicated the presence of polysulfides in experiments with S0 (Supplementary Fig. 164), supported by UV absorption peaks at 280 and 314 nm (Fig. 4b48,65). Experiments with S0 showed higher absorbances than experiments without S0, which indicates a higher abundance of dissolved polysulfides (Fig. 4b–d65). In the presence of colloidal S0, the absorbance of peaks characteristic of polysulfides was higher than in the presence of crystalline S0 (Fig. 4b–d, Supplementary Fig. 1). Generally, experiments with biogenic magnetite showed higher polysulfide abundances than equivalent experiments with abiogenic magnetite (Fig. 4b–d, Supplementary Fig. 1). Polysulfide abundances and the 314–280 nm absorbance peak ratio in all experiments increased over time (Fig. 4b–e).
a Increased absorbance in experiments with colloidal S0, particularly with abiogenic magnetite, likely due to the presence of colloidal FeS (see also Fig. 3a). b–d Absorption peaks at 280 and 314 nm showing the presence of dissolved polysulfides after 3, 10, and 35 days (b, c, d, respectively). Note that polysulfide abundances are higher in experiments with biogenic magnetite than abiogenic magnetite, with S0 than no S0, and with colloidal S0 than crystalline S0. e Ratios of absorbance peaks at 314 and 280 nm.
Scanning electron microscopy (SEM) and focused-ion-beam (FIB) milling
After 7 days of incubation, all experiments contained platy crystals characteristic of FeSm (Fig. 5a–f66,67). Experiments with abiogenic magnetite but without S0 further contained µm-sized cubic-euhedral pyrite (Fig. 5a). In the presence of both crystalline and colloidal S0, experiments with abiogenic magnetite contained octahedral-dendritic pyrite (Fig. 5b, c). No pyrite was observed in experiments with biogenic magnetite, irrespective of the presence of S0 (Fig. 5d–f). Since Raman spectroscopy and sequential extraction, but not µ-XRD, indicated the presence of pyrite (Figs. 1–3), the precipitates appear to be nano-crystalline.
a–f SEM images after 7 days. g–l SEM images after 21 days. FeSm formed in all experiments. Cubic-euhedral pyrite formed in experiments with neither organic matter (OM) nor S0 (a, g). In experiments with biogenic magnetite, no pyrite was observed after 7 days, irrespective of the presence of S0 (d–f). Dendritic-octahedral pyrite formed in experiments without OM but with the addition of S0 (b, c, h, i). Framboid-like pyrite spheroids only formed in experiments with OM and S0 after 21 days (k, l). All scale bars are 1 µm.
After 21 days of incubation (Fig. 5g–l), no morphological changes in the precipitates from experiments with abiogenic magnetite were observed (Fig. 5g–i). Also, pyrite remained undetected in experiments with biogenic magnetite but without S0 (Fig. 5j). However, samples from experiments with biogenic magnetite and crystalline and colloidal S0 contained ~3–5 µm-sized pyrite spheroids (Fig. 5k, l). FIB sections milled after 47 days of incubation revealed remnant internal grain boundaries within the pyrite spheroids, demonstrating that they consist of aggregates of nm-sized pyrite crystals (Fig. 6).
a overview of the FIB section. Note the presence of remnant grain boundaries near the edges of the spheroid (white arrows in b, white dotted lines in c).
Discussion
Magnetite dissolution
The absence of µ-XRD reflections and Raman bands characteristic for magnetite after 7 days (Figs. 1–2) suggests rapid sulfidation of the magnetite precursor in all experiments. This most likely proceeds via the reductive dissolution of magnetite driven by excess aqueous sulfide34,36, as supported by the initial increase in Fe(II)aq (Fig. 3a). Fe(II)aq likely represents the combined presence of dissolved Fe2+, colloidal FeS particles, and aqueous FeS complexes (Fig. 3a45,68). The presence of colloidal FeS in the supernatant is further supported by increased UV-Vis absorbance in these experiments (Fig. 4a). Accordingly, the higher Fe(II)aq concentration in experiments with colloidal S0 (Fig. 3a) is either due to an increased Fe2+ release from magnetite dissolution or a higher abundance of colloidal and/or aqueous FeS. An increased liberation of Fe2+ is readily explained by a faster dissolution rate of colloidal S0 compared to crystalline S069,70, which would release more reactive sulfur species into the system, promoting magnetite dissolution. This is also consistent with higher polysulfide abundances in the presence of colloidal S0 compared to crystalline S0 (Fig. 4b–d). Polysulfides generated in this process could also complex Fe2+, leading to a higher abundance of aqueous FeS species71.
We also observed lower initial Fe(II)aq in experiments with biogenic magnetite relative to equivalent setups with abiogenic magnetite (Fig. 3a). This could be due to the complexation of Fe(II)aq with organic molecules adsorbed to mineral surfaces (Supplementary Fig. 250). Alternatively, organic matter may passivate surfaces or promote the aggregation of magnetite and FeSm, lowering their dissolution rate and, thus, Fe(II)aq release47,51,72. The rapid decrease in Fe(II)aq after 3 days is likely due to the aggregation of colloidal FeS73. Subsequently, Fe(II)aq remains low because FeS is poorly soluble at pH 7.574.
Polysulfide formation
The higher abundance of polysulfides in the presence of S0 in our experiments suggests the oxidation of aqueous sulfide by S0 as a relevant process (Fig. 4b–d). Indeed, this process is known to yield stable polysulfides at pH > 770,75, which agrees with our experiment (pH 7.5). In contrast, the possible formation of polysulfides via oxidation of sulfide by Fe(III) in magnetite is most effective at neutral pH34,45,76 and hence is likely not the dominant mechanism in the case of our experiments. The higher abundance of polysulfides in experiments with colloidal S0 relative to crystalline S0 is likely due to the larger reactive surface of colloidal S0 (Fig. 4b–d69,70). Higher abundances of polysulfides in experiments with biogenic magnetite might suggest that organic matter drives the oxidation of aqueous sulfide to secondary S077, which then further reacts with sulfide to polysulfides.
Controls on pyritization rate
FeSm in our experiments co-exists with pyrite after 7 days and disappears after 21 days (Figs. 1–2, and 5), suggesting that pyritization proceeds via a FeSm precursor. The faster pyritization rate in experiments with added S0 (i.e., at a high polysulfide abundance, Figs. 3–4) indicates that pyrite in our experiments dominantly forms via the polysulfide pathway (Eq. (1)), consistent with previous magnetite sulfidation experiments under anoxic conditions34,39. Pyrite formation via the polysulfide pathway predicts a change in the polysulfide speciation (i.e., chain length) over time (Eq. (1)48). We speculate that the asymptotic increase in the 314–280 nm UV absorption peak ratio during our experiments (Fig. 4e) indicates an overall shift towards shorter polysulfide chain lengths, although individual polysulfide species cannot be discriminated with this technique alone.
Pyritization rates in experiments with biogenic magnetite were systematically slower than in equivalent setups with abiogenic magnetite, irrespective of the addition of S0 (Fig. 3). This is consistent with previous studies demonstrating an inhibitory effect of organic compounds on pyrite formation47,49,51,52 and demonstrates that organic matter has an additional control on reaction rates. Organic matter may protect S0 or FeSm against dissolution, potentially resulting in a decreased formation of polysulfides and, consequently, pyrite78,79. Moreover, organic matter sulfurization may act as a sink for polysulfides in experiments with biogenic magnetite, which would not be available for pyrite formation80. However, biogenic magnetite experiments showed increased abundances of polysulfides at slower pyritization rates (Figs. 3–4); hence, pyritization is not limited by polysulfide abundance. More likely, pyritization is inhibited by the sorption of organic matter to FeSm, decreasing mineral reactivity towards aqueous (poly)sulfide and limiting its aggregation and/or growth47,79. This, in turn, may slow down FeSm transformation to pyrite, especially at the nm scale81. This likely explains the inhibition of pyrite formation in the experiment with biogenic magnetite and no S0.
Rate control on pyrite morphology
In our experiments with abiogenic magnetite, there is a clear relationship between pyritization rate and morphology (Figs. 5 and 7). Octahedral-dendritic pyrite formed in the presence of S0 and at faster pyritization rates are morphologically identical to previously reported pyrites from sulfidation of abiogenic magnetite (Figs. 5b, c, h, i and 734). These crystals likely reflect high degrees of supersaturation, resulting in rapid nucleation34,82,83. In contrast, cubic-euhedral pyrite is generally associated with lower degrees of supersaturation and slower growth rates, allowing for well-developed crystal faces (Fig. 782). This is consistent with µ-XRD data, showing higher degrees of crystallinity than octahedral-dendritic pyrite produced in experiments with abiogenic magnetite and S0 (Fig. 1).
Magnetite is reductively dissolved by aqueous HS- (and H2S, not shown), releasing Fe2+ (and minor Fe3+, not shown), which reprecipitates as Fe(III)-FeSm. a Sulfidation of magnetite in the presence of OM but without S0 yields the slowest pyritization rates, resulting in nanoparticulate pyrite (not observed in SEM). b Without OM and S0, pyrite growth is slow, yielding cubic-euhedral pyrite. c In the presence of OM and S0, the pyritization rate is high, and OM mediates the formation of pyrite spheroids. d In the absence of OM but in the presence of S0, pyritization rates are the highest, yielding octahedral-dendritic pyrite. All scale bars are 1 µm.
The slower pyrite growth rates in our experiments with abiogenic magnetite and without S0 likely resulted from the lower abundance of polysulfides (Fig. 4b–d, Supplementary Fig. 1). Notably, the resulting cubic-euhedral pyrite in this study exhibits a distinctly different habitus than octahedral-dendritic pyrite that formed in previous magnetite sulfidation experiments at equivalent conditions (sulfide/Fe = 4, 62 mM S0) but slightly lower pH (~734 vs. 7.5 in the present study). This effect may be due to pH-dependent polysulfide formation in magnetite suspensions. In our experiments at pH 7.5, the surface-mediated polysulfide formation was muted76, possibly yielding an overall lower abundance of polysulfides than at pH 7. This may have inhibited the dominant polysulfide pathway for pyrite formation in our experiments at pH 7.5 without S0, yielding slower pyritization rates. Hence, this highlights that variations of only 0.5 pH units can substantially affect pyrite morphology.
Influence of organic matter on pyrite morphology
Biological organic matter, such as cell walls, microbial extracellular polymeric substances, or intracellular materials, can provide nucleation sites and templates for pyrite formation55,56,59. Furthermore, organic compounds may promote pyrite spheroid nucleation in anoxic experimental systems by increasing Eh59, substantially influencing pyrite morphology84. Organic matter also appears to strongly control pyrite morphology in our experiments. For instance, the slowest pyritization rates were observed in experiments with biogenic magnetite but without S0 (Fig. 3). Here, pyrite was evidenced with Raman spectroscopy, µ-XRD, and sequential extraction but is not visible in SEM even after 21 days, supporting slow growth to only very small particle sizes (Figs. 5 and 7). Organic matter was suggested to inhibit the growth and transformation of ferrihydrite in the presence of Fe(II) or sulfide via particle aggregation and Ostwald ripening47,53,85. Possibly, a similar mechanism affects nanoparticulate pyrite or its precursors, such as FeSm, in our experiment. On the other hand, experiments with biogenic magnetite and S0 contained ~3–5 µm-sized pyrite spheroids after 21 days, while no such spheroids were observed after the sulfidation of abiogenic magnetite (Figs. 5 and 7). Based on our data, it cannot be resolved whether templating effects or organic matter-induced kinetic effects primarily drive pyrite spheroid formation. However, the pyritization of biogenic magnetite likely proceeds via a complex interplay of these factors, with organic matter playing a key role in controlling pyrite morphology.
Spheroids vs. framboids—similarities and differences
Framboidal pyrite is commonly used to track microbial sulfur cycling in modern and ancient environments. This, however, requires that the analyzed precipitates are pristine products of primary geomicrobiological processes. While lacking the diagnostic raspberry-like internal texture, pyrite spheroids in our experiment approximate pyrite framboids in anoxic and sulfidic sediments concerning the overall spherical habit, aggregational texture, and size (~3–5 µm)86. Moreover, the organic matter-mediated formation of pyrite spheroids in our experiment is broadly analogous to mechanisms proposed for generating pyrite framboids in sedimentary deposits, including sulfate-reducing biofilms or microbial mats54,55,56. This suggests that in the presence of biogenic (i.e., organic matter-associated) precursor iron minerals and S0, framboid-like pyrite spheroids could form in the same environments as true framboids. Moreover, petrographic observations suggest that diagenetic and hydrothermal alteration of pyrite framboids can induce infilling and recrystallization processes that drive their textural evolution towards spherical precipitates that do not exhibit pristine internal textures87. Indeed, some pyrite in ancient rocks described as framboids show an overall spherical habit but lack the internal texture of pristine framboids (e.g.,10,57,88). While our findings do not refute that these precipitates are indeed infilled or recrystallized framboids10,89, we suggest that some of such pyrite may have been originally pyrite spheroids, particularly in hydrothermal environments.
Spheroids as biosignatures for iron-cycling microorganisms?
We demonstrated that the hydrothermal sulfidation of biogenic magnetite can drive the formation of framboid-like pyrite. Consistent with previous experimental studies59, this indicates that microbial sulfur cycling is not necessarily the critical mechanism for forming framboid-like pyrite, meaning that such precipitates may not be specific biosignatures for sulfur-cycling microorganisms. Instead, framboid-like pyrite may be the product of the diagenetic transformation of biogenic iron minerals, such as magnetite produced by dissimilatory Fe(III)-reducing prokaryotes or magnetotactic bacteria, under sulfidic conditions (Fig. 7c). Framboid-like pyrite may result from the sulfidation of biogenic magnetite irrespective of whether reduced sulfur species are biogenic (i.e., from microbial sulfur cycling) or abiogenic (e.g., volcanogenic) in origin. This means framboid-like pyrite may be a promising taphonomic fingerprint of precursor biominerals resulting from microbial iron cycling, particularly in hydrothermal sulfide systems.
Conclusions
We demonstrated that sulfidation of abiogenic and biogenic magnetite yields pyrite under sulfidic hydrothermal conditions. Pyritization rates and pyrite morphology were strongly controlled by S0 (S0 promoting pyritization; cubic-euhedral without S0, octahedral-dendritic with S0), pH (octahedral-dendritic at pH 7, cubic euhedral at pH 7.5), and organic matter (inhibiting pyritization). Notably, S0 and organic matter promoted the formation of ~3–5 µm pyrite spheroids that resembled pyrite framboids, demonstrating that framboid-like pyrite can form via the hydrothermal sulfidation of biogenic magnetite under sulfidic conditions. This suggests that some framboid-like pyrite in ancient rocks may represent original pyrite spheroids rather than recrystallized or infilled pyrite framboids, particularly in hydrothermal deposits. Moreover, our study highlights the need to constrain the impact of diagenetic processes on pyrite morphologies. Framboid-like pyrite may represent a taphonomic product from the sulfidation of biogenic magnetite. Therefore, framboid-like pyrite is not only a potential fingerprint of microbial sulfur cycling but can also record microbial iron cycling in hydrothermal systems.
Methods
Starting materials
For experiments with abiogenic magnetite (i.e., without organic matter), we synthesized magnetite nanoparticles in an N2-filled anoxic chamber according to previously described procedures34. For experiments with biogenic magnetite (i.e., with organic matter), we prepared magnetite nanoparticles via dissimilatory Fe(III)-reduction of 2-line ferrihydrite by Geobacter sulfurreducens. The 2-line ferrihydrite was prepared by reaction of Fe(NO3)3·9H2O (40 g) with KOH (1 M) until pH 7.090. The material was centrifuged (26000 × g; 10 min) and washed three times in Milli-Q H2O to remove nitrate ions and then purged with N2 to remove O2. A dense culture of G. sulfurreducens was inoculated at 10% (v/v) in a total volume of 100 mL growth medium in a 200 mL serum bottle and closed with butyl stoppers. The growth medium contained 30 mM NaHCO3, 25 mM Na acetate, 40 mM Na fumarate, and 1 mL each of SL-10 trace element solution, seven vitamin solution, and selenite-tungstate solution91. In the late exponential phase (after ~48 h, OD600~0.5), the cells were centrifuged at (5300 × g; 20 min) and washed in 50 mL of 10 mM HEPES buffer solution (pH 7.0) three times. The resulting cell pellets were resuspended in 10 mM HEPES buffer solution and then added at OD600 = 0.38 to a Fe(III)-reduction medium containing 10 mM HEPES buffer, 25 mM Na acetate, and 50 mM 2-line ferrihydrite at 30 °C for three days. The dissimilatory Fe(III)-reduction was conducted in 25 mL total volume in 50 mL serum bottles closed with butyl stoppers. Anoxic and sterile conditions were maintained during all steps in the preparation of biogenic magnetite.
Both abiogenic and biogenic magnetite were washed by holding the particles in place, placing a hand-magnet to the outside of the serum bottle, decanting the supernatant, adding ~80 mL O2-free ultrapure H2O (Milli-Q, Merck Millipore), and sonicating for 5 min. This procedure was repeated two times. The total organic carbon contents (TOC) of the abiogenic and biogenic magnetite suspensions were determined as the sum of the dissolved organic carbon (DOC) in the liquid phase and the organic carbon content of the solid phase (Supplementary Table 1). After centrifugation at 12,100 × g for 5 min, the DOC of the liquid phase was analyzed using a Multi N/C analyzer 2100S (Analytik Jena GmbH) as the non-purgeable organic carbon after acidification with 50 µL of 2 M HCl. For organic carbon analyses of the solid phase, samples were dried at 50 °C and powdered with a ball mill. Double determination analysis was conducted using a Vario Cube Elemental Analyzer (Elementar Analysesysteme GmbH), and quantification was done using the sulfanilamide standard. The resulting TOC of the abiogenic and biogenic magnetite suspensions were 0.98 mM and 9.29 mM, respectively. The average crystallite sizes of the synthesized abiogenic and biogenic magnetite (confirmed by µ-XRD; Supplementary Fig. 2), as calculated using the Scherrer equation92, were 12 nm and 9 nm, respectively.
Artificial seawater was prepared using 17.30 g/L NaCl, 8.61 g/L MgCl2•6H2O, 0.03 g/L MgSO4•7H2O, 0.99 g/L CaCl2•2H2O, 0.39 g/L KCl, 0.06 g/L KBr, 0.25 g/L NH4Cl, and 1.85 g/L NaHCO3. The pH of the resulting solution was adjusted to 7.0 using 1 M HCl, and dissolved O2 was degassed by purging with 50/50 N2/CO2. An anoxic 1 M sulfide solution was made by dissolving Na2S in O2-free ultrapure H2O. Colloidal S0 was prepared by dropwise addition of 10 mL concentrated H2SO4 to 30 mL 3 M Na-thiosulfate [Na2S2O3 × 5H2O] solution, which was immersed in an ice bath. Precipitation of colloidal S0 in this process yielded a yellow suspension. The aggregation of colloidal S0 was induced by the addition of 40 mL saturated NaCl solution. To remove excess NaCl, the colloidal S0 was allowed to settle overnight, the supernatant was removed, and 50 mL of 2% NaCl was added. This process was repeated three times. The resulting suspension was transferred to a serum bottle and purged with N2 to remove O2. The concentration of the colloidal S0 stock was determined gravimetrically after drying an aliquot at 60 °C.
Experimental setups
The preparation of incubation experiments, sampling, and sample preparation for analysis were conducted in an N2-filled anoxic chamber. Batch experiments were prepared with total volumes of 50 mL in 100 mL-volume serum bottles closed with butyl stoppers to prevent the presence of oxygen. We used a minimum of two experimental replicates for chemical analysis (pH, sequential iron extraction). At least one additional replicate per setup was prepared for mineralogical analysis (Raman spectroscopy, µ-XRD) and SEM.
The magnetite suspensions and the sulfide solution were added to the artificial seawater at 60 mM sulfide and 15 mM iron (4:1 molar ratio). This mixing ratio resulted in 0.14 mM and 1.3 mM added TOC from abiogenic and biogenic magnetite, respectively. To each experimental setup, 100 mM MOPS buffer was added, which resulted in an average initial pH of 7.46 ± 0.06 (Supplementary Fig. 3). During the experiment, the pH remained constant within ±0.1 pH units (i.e., decreased to 7.38 ± 0.03; Supplementary Fig. 3). For both abiogenic and biogenic magnetite experiments, we prepared two additional setups that further contained 62 mM of commercially available crystalline S0 (100 mg, Sigma–Aldrich, product # 13803) or pre-synthesized colloidal S0 (suspended in 2% NaCl solution), respectively. Light microscopy observations indicate that crystalline S0 particles were ~30 µm while colloidal S0 particles were ≤5 µm in size. All serum bottles were incubated at 80 °C.
Geochemical analyses
Aliquots (0.5 mL) of the mineral suspension were centrifuged for 5 min at 12,100 × g to separate the minerals from the aqueous phase (this phase contains both the combined dissolved and colloidal iron that did not settle during centrifugation). Concentrations of Fe2+ in the aqueous phase and total iron in the solid phase were quantified spectrophotometrically using the ferrozine assay93. Supernatants were acidified with 1 M HCl before analysis. Sequential iron extraction of the solid phase using 6 M HCl (reactive iron minerals: magnetite, mackinawite, and greigite) and 8 M HNO3 (pyrite) was used to determine the degree of pyritization over time94,95. Extraction with 6 M HCl was conducted for 24 h in an anoxic chamber in the presence of Ti(III)-citrate to prevent oxidation of dissolved sulfide to S0, which could reduce iron extraction yields96. Solid residues from the 6 M HCl extraction step were extracted with 8 M HNO3 for >2 h. Centrifuged aliquots of the liquid phase were analyzed in duplicates for the presence of polysulfides via UV-Vis spectroscopy in 96-well plates using a spectral range of 250–500 nm. The resulting spectra were normalized using a Milli-Q blank.
µ-X-ray diffraction (µ-XRD)
Aliquots for µ-XRD measurements were taken in an N2-filled anoxic chamber. Mineral pellets were harvested by centrifugation and washed three times with anoxic ultrapure water to remove residual salts before drying. Dry samples were stored in N2-filled preserving jars until µ-XRD analysis under ambient atmospheric conditions97,98. µ-XRD was performed on dry material using a Bruker’s D8 Discover GADDS XRD2 micro-diffractometer equipped with a standard sealed tube with a copper-anode (Co Kα radiation, λ = 0.179 nm) at 30 kV/30 mA. The total time measurement was 240 s at two detector positions (15° and 40°). Phase identification was validated using the Match! Software for phase identification from powder diffraction (Match!, Crystal Impact, Bonn, Germany, version 3.11.5.203) with the Crystallography Open Database (COD-Inorg REV211633 2018.19.25).
Raman spectroscopy
Aliquots from suspended samples were dried onto glass slides in an anoxic chamber. Glass slides were transported to the instrument in N2-filled jars. Raman spectra were acquired with an Alpha 500R Confocal Raman Microscope (WITec GmbH, Ulm, Germany), which was equipped with a 532 nm excitation laser, a UHTS 300 spectrometer, and a DV401-BV CCD camera. The optical grating was 600 g/mm for recording the spectra from 0 to 3790 cm−1. A 40× objective with a numerical aperture of 0.6 was used (EC Epiplan-neofluor, Carl Zeiss, Germany). The laser power was adjusted to ≤1 mW using an optical power meter (PM100D, Thorlabs GmbH, Dachau, Germany) to avoid heat-induced mineral transformation. Three spots were analyzed per sample using up to 10 integrations of 10–20 s each. Spectra from these three spot measurements were combined into a composite spectrum, and relative intensities were normalized to 100. Pyrite was identified using the software CrystalSleuth, the RRUFF database (https://rruff.info/; accessed 16 August 2023), and Fe(III)- FeSm was compared to reference patterns from Bourdoiseau et al.63.
Scanning electron microscopy (SEM) and focused-ion-beam (FIB) milling
Aliquots from experimental duplicates were pooled and washed three times with anoxic Milli-Q water. These samples were dried onto a carbon adhesive tab attached to an aluminum stub in an anoxic chamber. Once dry, the samples were coated with 8 nm of gold using a BAL-TEC SCD 005 sputter coater to reduce charging effects during analysis. Morphological characterization of experimental products was performed using a Crossbeam 550L SEM (Zeiss, Oberkochen, Germany) operating at an acceleration voltage of 2 kV and working distances of 5.2 mm. All micrographs were taken using the Secondary Electron Secondary Ion (SESI) detector.
FIB milling was performed on a Zeiss Crossbeam 550L. A SEM stub was coated with a thin layer of Tempfix (Plano G3305). The coated stub was held at a temperature of approximately 40 °C and the anoxically dried sample was sprinkled onto its surface. After reaching room temperature, the sample was sputter-coated with 8 nm of platinum. A cross-section through the object of interest was made using the 300 pA–30 kV FIB probe. In a second step, the surface of the cross-section was polished using the 2 pA–30 kV FIB probe. Images were generated using the InLens detector at an acceleration voltage of 5 kV and a probe current of 100 pA.
Reporting summary
Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.
Data availability
The data supporting this study’s findings are available within the paper and its Supplementary Materials and through an online repository using the following link: https://doi.org/10.6084/m9.figshare.25539925. Any additional information is available from the corresponding authors upon reasonable request.
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Acknowledgements
We thank François Guyot and two anonymous reviewers for their constructive feedback. This study was supported by the DFG (SPP 1833, Emmy Noether Programme; DU 1450/3-2, DU 1450/7-1; J.P.D., E.R.; INST 37/1027-1 FUGG; A.K.) as well as by the German Excellence Strategy of the German Federal and State Governments (EXC2124, 390838134; Tübingen Structural Microscopy Core Facility; A.K., M.M., S.F., J.S.). We thank James M. Byrne for advice on preparing biogenic magnetite and Prachi Joshi, Aude Picard, and Julie Cosmidis for helpful discussions on the experimental design. Jorinel-Manuel Domingos kindly provided colloidal S0. Eva Voggenreiter and Johann Holdt helped with TOC analysis. Dominique J. Lunter and Hans Schönfelder are thanked for their assistance with Raman spectroscopy.
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E.R., M.M., A.K. and J.-P.D. planned and designed the experiment. E.R. and T.H.C. prepared abiogenic and biogenic magnetite. E.R. conducted the experiments and analyzed the data. J.S. and S.F. performed FIB and SEM analysis. T.H.C. performed µ-XRD analysis and prepared FIB and TOC samples. All authors contributed to the discussion of results and writing.
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Runge, E., Mansor, M., Chiu, T.H. et al. Hydrothermal sulfidation of biogenic magnetite produces framboid-like pyrite. Commun Earth Environ 5, 252 (2024). https://doi.org/10.1038/s43247-024-01400-z
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DOI: https://doi.org/10.1038/s43247-024-01400-z
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