Cellular remains in a ~3.42-billion-year-old subseafloor hydrothermal environment – Science Advances

To understand the origin and nature of the studied filaments, morphological and chemical signatures require evaluation regarding biogenicity (section S4). The reconstructed ecological setting provides further constraints on interpreted metabolic pathways.

Filamentous microfossils

Although a plausible biological morphology alone is not decisive proof of the microbial origin of the filamentous structure, it is a required criterion for identifying microbial fossils (section S4) (3, 2325). Several morphological features of the studied filaments are notably similar to other permineralized microfossil examples found throughout the geological record [e.g., (4, 2426)]. Disarticulation (Fig. 3A and fig. S8, E and F) is a common attribute of fossilized microbial filaments [e.g., (4, 2426)] and could reflect either or both structural (i.e., cell division points) (23, 26) and taphonomic discontinuities (i.e., due to compressions or less preserved and degraded remains) (2, 23, 27). High morphological 3D fidelity of the filament preservation is consistent with very early and rapid silicification [e.g., (24, 28, 29)], which is to be expected of Paleoarchean silica-saturated hydrothermal systems (10, 19).

All of the filaments we analyzed here are embedded in (α-quartz) chert (Figs. 3, B and C, and 4, B and C) and are composed of moderately ordered carbon (Fig. 4D), consistent with ancient permineralized kerogenous cellular remains (2325). In addition to having a kerogenous composition [also supported by the presence of H, N, and C-N heteroatoms; Fig. 2; e.g., (30)], we revealed the nested distribution of (spectrally) different types of molecular carbonaceous compounds associated with some of the filaments. Although the diffusion of the cellular material along quartz crystal boundaries is a known taphonomic or diagenetic effect that could generate around the fossils themselves specific secondary textural patterns including carbonaceous halos, piliform or saw-tooth structures, and semihollow mold [e.g., (27, 31)], evidences of such processes—i.e., quartz particles wrapped in the kerogen of the filament outer walls and/or carbon redistributed throughout the quartz matrix in the vicinity of the filament periphery—were not observed by high–lateral resolution, high–spatial resolution, and high–spectral resolution investigations (Fig. 3B, movie S1, and fig. S11.1). Furthermore, filaments were not generated by carbonaceous compounds coating crystal surface or intragranularly displaced during recrystallization [e.g., (31)]. The carbonaceous external layer could plausibly represent remnants of a cell wall, a cell membrane, an extracellular sheath or envelope, or an extracellular polymeric substance (EPS) component, whereas the core of the “sheathed” filaments could be condensed intracellular or cytoplasmatic matter. In such a case, the nested correlation of cell and outer/extracellular features comprised of different forms of CM would reflect an ultrastructural (spectral) elaboration consistent with a cellular origin (23), and the local discontinuity of the extracellular features could likely reflect early microbial degradation immediately before early fossilization. The presence of a thin localized, although partially discontinuous, external C layer that is structurally distinct from the kerogenous filament cores and the CM disseminated in the silica matrix (Fig. 3, B and C, and section S5) could reflect differences in the composition of the organic precursors and could be consistent with preservation of the remains of sheath-like or cell wall–like structures (32). The nanoscale carbonaceous particles dispersed in the chert matrix (Fig. 3B and section S5) display distinct Raman spectra and likely represent carbonaceous components frequently observed in chert cement (7, 33, 34). Kerogenous composition of the filaments and carbonaceous nanoscale particles is consistent with low-grade metamorphic overprinting of the central BGB (section S5) (5).

The chemical composition of the filaments is consistent with a kerogenous nature and includes most of the major bioessential elements (C, H, O, and N in Fig. 2 and S in fig. S13). The absence of P could be the result of scavenging or leaching of this bioessential element. Moreover, postdepositional taphonomic reworking of heteroatoms would concentrate decay-resistant biopolymers that covalently bond S, N, and C [e.g., (35)]. The homogeneous distribution of trace amounts of S (fig. S13) associated with the kerogen in the filaments, along with the sulfide XANES K-edge at 2473.5 eV, suggests the presence of an organic heterocyclic sulfide as previously detected in other Precambrian microfossils (35). Organic linear and heterocyclic sulfides are purportedly formed by the aromatization of organics during thermal metamorphism, which stabilizes kerogen (36).

The presence of Ni-organic compounds in the filaments (Fig. 5) is consistent with primordial metabolisms (37) and not unexpected, given the high bioavailability of Ni on the reducing early Earth and in situ Ni trace detection in ~3.33-Ga-old organic matter (38). The cellular levels of Ni enzymes intrinsic to the methanogenic and methanotrophic metabolic pathways of modern microbes (3941) are particularly high, as are their Ni contents (4245). Ni enzymes, commonly used in anaerobic metabolisms, have also been highly conserved from molecular evolution over geological time (37, 46). Furthermore, the evidence for possible Ni-organic complexes with mixed II/III Ni valencies (47) is consistent with cofactors of inactivated enzymes involved in methane-metabolizing pathways. The measured Ni concentrations in the filaments (2.78 × 107 ± 1.95 × 106 at μm−3 equivalent to 0.46 ± 0.03 mM) (Fig. 5A) similar to the Ni contents reported for modern methanogenic microbes [e.g., 0.44 ± 0.04 mM in (45); see also (4244, 48)] are also consistent with the presence of methanogens and methanotrophs. In addition, several examples of methane-cycling microorganisms with slender (>1-μm) straight or curved filaments with walls, septa, or extracellular envelopes (e.g., Thermofilum, Methanosaeta, and Crenothrix) are known.

The filaments satisfy the commonly accepted biogenicity, indigenicity, and syngenicity criteria (section S4). The studied filaments also differ from known abiotic pseudofossils (section S4) in the specific combination of their site of occurrence, 3D morphological complexity, kerogenous nature, spectrally observed ultrastructures, and their specific metal-organic signature. Although biomorphs, produced in the absence of any direct biological activity under geochemical conditions that could have existed on early Earth [e.g., (49, 50)], must be considered when evaluating the biogenicity of putative early trace of life, their features with the various attributes of the filaments described here are currently not known (section S4). Possibly the strongest evidence for the biogenicity of the studied filaments is their occurrence in specific associations (single or in clusters) within different parts of the vein microhabitat and in association with biofilms.

Although cellular fossils of archaeal methanogens and methanotrophs have not yet been reported in the Paleoarchean record (2, 3) and Paleoarchean geochemical evidence (carbon isotopes) for microbially produced methane is limited (51), methane-utilizing metabolic pathways are commonly recognized as ancient in origin [e.g., (3, 46)]. Despite the demonstrated fossilization potential of Archaea [e.g., (29)], their fossil record is restricted to the Phanerozoic (2, 3, 52). Our findings could possibly extend this record back to 3.42 Ga.

Archean ecological habitat within a subseafloor hydrothermal system

The fossil assemblage we described here flourished in a paleo-subseafloor setting at the interface of a carbonated ultramafic lapillistone and silica-oversaturated hydrothermal fluid (schematic model in section S3). The hydrothermal processes, likely related to cooling of the underlying volcanic and volcaniclastic rocks following eruption and deposition on the seafloor, generated widespread low-temperature [≤150°C; (8, 10)] diffuse flow systems of seawater chemically modified during water-rock interaction. At ~3.4 Ga, seawater was anoxic (53), less alkaline [~neutral pH; (54)], and possibly warmer than today [<40°C; (55)]. Its interaction with fresh ultramafic rock at depth would have made it more alkaline (8) and enriched in biophilic metals such as Ni (10). The high pH of subsurface fluids is indicated by pervasive carbonatization of ultramafic rocks at depth, with secondary carbonate having a carbon isotopic composition that indicates that Ccarbonate was derived from seawater (section S3). A few meters below the paleoseafloor (section S2), large-scale mixing of subsurface fluids with colder and less alkaline seawater following hydraulic fracturing would likely have resulted in the replacement of earlier-formed carbonate by secondary silica, which itself presumably precipitated upon a drop in pH, during ongoing fracturing events that subsequently established new links with the seafloor. Zones with strong geochemical gradients that enhanced water-rock interactions are typically regarded as suitable ecological niches for communities of lithoautotrophs in both past and present subseafloor settings (14, 37).

The irregularity of the upper vein margins suggests dissolution and silica replacement of the host rock, whereas the lower vein margins could have been protected from dissolution by the presence of an actively metabolizing microbial biofilm community that colonized the accretionary surface of the vein wall (Ib). That filament clusters were only found near the end of cusp-shaped cavities of the hanging walls of the vein and that single filaments were associated with what appear to be mottled CM relicts of biofilm on the vein floor clearly indicate variations in the ambient physicochemical conditions and thus multiple potential microbial microhabitats within the veins. This is mirrored by modern vent microbial communities, which are distributed, due to selective physicochemical forces, within distinct macro- and microenvironmental vein settings (12). These environments—typified by moderate hydrothermal temperature, abundant availability of essential nutrients, and steep redox and pH gradients—would have provided the necessary ingredients and free energy to sustain biofilms comprised of acetogens, methanogens, methanotrophs, and heterotrophs (14, 37, 56). The presence of specific Ni-organic compounds associated with the filaments is consistent with methane-cycling metabolic pathways known to dominate subsurface microbial communities in ultramafic environments (57). The CM of subsequent vein-fill generations lacking cellular remains likely originated from planktonic and benthonic material entrained in the downward flow of sediment-laden seawater (section S3) (8, 20, 34). CM is also found in the lapillistone and dispersed within the chert cement (section S2) and may have formed abiotically, as hydrocarbons derived from subsurface serpentinization reactions and thermal alteration of carbonaceous seafloor sediments [e.g., (58, 59)]. Hydrocarbons would have become entrained in such hydrothermal systems and could have provided further support of methane-cycling microbial assemblages.

In this work, a suite of converging and mutually supportive evidence indicative of biogenicity (morphology and chemical composition) and a favorable ecological setting along with meeting endogenicity and syngenicity criteria (3) was established for filaments in a habitable Archean subsurface ultramafic environment. This discovery of microfossils extends knowledge of the early subsurface fossil record and provides a strong case for the importance of subsurface hydrothermal systems as an abode for early life (11, 14). These findings provide the oldest direct evidence for subsurface methane-cycling microorganisms, most likely methanogens, consistent with their expected antiquity based on carbon isotope analysis of fluid inclusions (51) and molecular evidence (46).

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