David Andrew Fike

Chemosymbiosis may have been a key driver of early animal evolution and diversification. Yet evidence for animal–microbe nutritional partnerships in the fossil record of early metazoans remains scarce, largely owing to the limited availability of robust geochemical proxies and suitable fossilization pathways. Here, we report extremely low molybdenum isotope (δ ⁹⁸ Mo) values in pyritized fossils of the terminal Ediacaran Conotubus , a nonbiomineralized cloudinomorph representing some of the earliest metazoans. Such low δ ⁹⁸ Mo values are otherwise only known in modern cold-seep chemosymbiotic tubeworms hosting sulfur-oxidizing bacterial symbionts. Homogeneously low δ ³⁴ S signatures of fossils indicate that rapid pyritization in early diagenesis under euxinic taphonomic settings preserved primary Conotubus chitinous δ ⁹⁸ Mo. Substantial δ ³⁴ S fractionation relative to seawater sulfate and high Δ ³³ S values indicate that active microbial H ₂ S oxidation occurred within their habitat. Our findings provide evidence that Conotubus may have engaged in chemosymbiosis with sulfur-oxidizing bacteria—the earliest geochemically supported case in the fossil record. This trophic strategy likely enabled Conotubus to thrive in the redox-stratified Ediacaran ocean where sulfide and oxidants coexisted, facilitating its ecological success.

Bulk-rock sulfur isotope data from pyrite in the ~2.1 billion-year sedimentary rocks of the Francevillian Basin, Gabon, have underpinned ideas about initial oxygenation of Earth’s surface environments and eukaryote evolution. Here, we show, using micro-scale analytical methods, that the bulk sulfur isotope record represents progressive diagenetic modification. Our findings indicate no significant change in microbial sulfur cycling processes and seawater sulfate composition throughout that initial phase of atmosphere-ocean oxygenation of Paleoproterozoic time. This offers an alternative view of Earth system evolution during the transition from an anoxic to an oxic state and highlights the need for a judicious reappraisal of conceptual models using sulfur isotope data as primary depositional signals linked to global-scale biogeochemical processes.

Reconstructions of coupled carbon, oxygen, and sulfur cycles rely heavily on sedimentary pyrite sulfur isotope compositions (δ ³⁴ S _pyr ). With a model of sediment diagenesis, paired with global datasets of sedimentary parameters, we show that the wide range of δ ³⁴ S _pyr (~100 per mil) in modern marine sediments arises from geographic patterns in the relative rates of diffusion, burial, and microbial reduction of sulfate. By contrast, the microbial sulfur isotope fractionation remains large and relatively uniform. Over Earth history, the effect of increasing seawater sulfate and oxygen concentrations on sulfate and sulfide transport and reaction may explain the corresponding increase observed in the δ ³⁴ S offset between sulfate and pyrite. More subtle variations may be related to changes in depositional environments associated with sea level fluctuations and supercontinent cycles.

Reconstructions of past environmental conditions and biological activity are often based on bulk stable isotope proxies, which are inherently open to multiple interpretations. This is particularly true of the sulfur isotopic composition of sedimentary pyrite (δ ³⁴ S _pyr ), which is used to reconstruct ocean-atmosphere oxidation state and track the evolution of several microbial metabolic pathways. We present a microanalytical approach to deconvolving the multiple signals that influence δ ³⁴ S _pyr , yielding both the unambiguous determination of microbial isotopic fractionation (ε _mic ) and new information about depositional conditions. We applied this approach to recent glacial-interglacial sediments, which feature over 70‰ variations in bulk δ ³⁴ S _pyr across these environmental transitions. Despite profound environmental change, ε _mic remained essentially invariant throughout this interval and the observed range in δ ³⁴ S _pyr was instead driven by climate-induced variations in sedimentation.

The sedimentary pyrite sulfur isotope (δ³⁴S) record is an archive of ancient microbial sulfur cycling and environmental conditions. Interpretations of pyrite δ³⁴S signatures in sediments deposited in microbial mat ecosystems are based on studies of modern microbial mat porewater sulfide δ³⁴S geochemistry. Pyrite δ³⁴S values often capture δ³⁴S signatures of porewater sulfide at the location of pyrite formation. However, microbial mats are dynamic environments in which biogeochemical cycling shifts vertically on diurnal cycles. Therefore, there is a need to study how the location of pyrite formation impacts pyrite δ³⁴S patterns in these dynamic systems. Here, we present diurnal porewater sulfide δ³⁴S trends and δ³⁴S values of pyrite and iron monosulfides from Middle Island Sinkhole, Lake Huron. The sediment–water interface of this sinkhole hosts a low‐oxygen cyanobacterial mat ecosystem, which serves as a useful location to explore preservation of sedimentary pyrite δ³⁴S signatures in early Earth environments. Porewater sulfide δ³⁴S values vary by up to ~25‰ throughout the day due to light‐driven changes in surface microbial community activity that propagate downwards, affecting porewater geochemistry as deep as 7.5 cm in the sediment. Progressive consumption of the sulfate reservoir drives δ³⁴S variability, instead of variations in average cell‐specific sulfate reduction rates and/or sulfide oxidation at different depths in the sediment. The δ³⁴S values of pyrite are similar to porewater sulfide δ³⁴S values near the mat surface. We suggest that oxidative sulfur cycling and other microbial activity promote pyrite formation in and immediately adjacent to the microbial mat and that iron geochemistry limits further pyrite formation with depth in the sediment. These results imply that primary δ³⁴S signatures of pyrite deposited in organic‐rich, iron‐poor microbial mat environments capture information about microbial sulfur cycling and environmental conditions at the mat surface and are only minimally affected by deeper sedimentary processes during early diagenesis.

Understanding variation in the sulfur isotopic composition of sedimentary pyrite (δ³⁴S_pyr) is motivated by the key role of sulfur biogeochemistry in regulating Earth’s surface oxidation state. Until recently, the impact of local depositional conditions on δ³⁴S_pyr has remained underappreciated, and stratigraphic variations in δ³⁴S_pyr were interpreted mostly to reflect global changes in biogeochemical cycling. We present two coeval δ³⁴S_pyr records from shelf and basin settings in a single sedimentary system. Despite their proximity and contemporaneous deposition, these two records preserve radically different geochemical signals. Swings of ~65‰ in shelf δ³⁴S_pyr track short-term variations in local sedimentation and are completely absent from the abyssal record. In contrast, a long-term ~30‰ decrease in abyssal δ³⁴S_pyr reflects regional changes in ocean circulation and/or sustained pyrite formation. These results highlight strong local controls on δ³⁴S_pyr, calling for reevaluation of the current practice of using δ³⁴S_pyr stratigraphic variations to infer global changes in Earth’s surface environment.

The goal of this project is to develop a new analytical platform for the rapid, high-precision determination of elemental and stable isotopic composition of microbial populations at sufficiently high spatial resolution to localize and quantitatively map bioessential elements within cells. The analytical approach makes use of a technique, secondary ion mass spectrometry (SIMS), where the sample is bombarded with a focused ion beam, generating secondary ions from the sample itself, which are electromagnetically focused onto a series of collectors. With enhanced ion source and detector capabilities, this instrument will be used to probe the uptake, assimilation, and sub-cellular localization of key elements, isotopes, and biomolecules in a suite of different model microbial systems (cyanobacteria, purple photosynthetic bacteria, and Methylobacterium), which are all promising systems for sustainable bioenergy production. The resulting data will be enable us to link together molecular-scale chemical and isotopic information with biological function to generate whole-cell, systems-level understanding that is currently not achievable using standard SIMS instruments.