Rapid pyritization in the presence of a sulfur/sulfate-reducing bacterial consortium

Abstract

Sedimentary pyrite (feS 2) is commonly thought to be a product of microbial sulfate reduction and hence may preserve biosignatures. However, proof that microorganisms are involved in pyrite formation is still lacking as only metastable iron sulfides are usually obtained in laboratory cultures. Here we show the rapid formation of large pyrite spherules through the sulfidation of Fe(III)-phosphate (FP) in the presence of a consortium of sulfur-and sulfate-reducing bacteria (SRB), Desulfovibrio and Sulfurospirillum, enriched from ferruginous and phosphate-rich Lake Pavin water. In biomineralization experiments inoculated with this consortium, pyrite formation occurred within only 3 weeks, likely enhanced by the local enrichment of polysulfides around SRB cells. During this same time frame, abiotic reaction of FP with sulfide led to the formation of vivianite (Fe 3 (po 4) 2 •8H 2 o) and mackinawite (feS) only. our results suggest that rates of pyritization vs. vivianite formation are regulated by SRB activity at the cellular scale, which enhances phosphate release into the aqueous phase by increased efficiency of iron sulfide precipitation, and thus that these microorganisms strongly influence biological productivity and Fe, S and P cycles in the environment. Pyrite (FeS 2) is the main sedimentary sink for sulfur over geological time scales. Because the burial of (di) sulfides leaves behind oxidized products, pyrite burial exerts a major control on the oxidation state of the ocean-atmosphere system 1-3. The ubiquitous occurrence of pyrite in marine and freshwater sediments 4-7 makes it a keystone for the reconstruction of past biogeochemical conditions at the Earth's surface. There are two generally accepted pathways for pyrite formation, both starting from an FeS (e.g. mackinawite) precursor: the polysulfide 8,9 pathway via which zero-valent sulfur acts as an oxidant for FeS producing FeS 2 via the non-obligate intermediate greigite (Fe 3 S 4) 10 , and the H 2 S pathway resulting in the formation of H 2 8,9,11. While sulfur-and sulfate-reducing bacteria (SRB) are the main source of sulfide (H 2 S or HS −) for FeS formation in sediments, their role in the formation of pyrite is still widely debated. Based on isotopic signatures (∂ 56 Fe and ∂ 34 S) in sedimentary pyrites, it has been suggested that pyritization can be driven by a combination of abiotic processes (diagenesis) and microbial Fe and S reduction 12,13. However, pyrite has rarely been obtained in mixed bacterial cultures 14,15 and even more rarely in pure cultures of SRB 16 , which instead promote the formation of metastable Fe sulfides such as amorphous FeS, mackinawite, pyrrhotite or greigite 17-20. These minerals are usually associated with cell walls or extracellular polymeric substances (EPS) produced by bacteria 18,19. A single study of pure cultures of D. desulfuricans 16 reported the formation of pyrite and marcasite from the sulfidation of Fe(III)-oxyhydroxide (goethite) after 3 to 6 months. This suggests that the presence of Fe(III) promotes the ...

Mechanisms of Pyrite Formation Promoted by Sulfate-Reducing Bacteria in Pure Culture

“…Although pyrite was only detected in the sediments and not in the water column, sulfate-rich enrichment cultures from this lake led to rapid pyrite formation after 21 days of culture (Berg et al, 2020). Here, our results demonstrate that the sole activity of Desulfovibrio (representing 80 % of the microbial consortium in the enrichment (Berg et al, 2020)) was able to promote pyrite formation. However, while, in the present study, pyrites occurred as infra micrometric spherules undetectable by X-ray diffraction after one month, pyrites produced within the Lake Pavin consortium were visible on diffractograms after only 21 days and occurred as beads of 1 µm in diameter (Berg et al, 2020).…”

“…The results of the present study demonstrate that Desulfovibrio desulfuricans alone had the ability to induce vivianite formation in the FP-nano condition, suggesting that sulfatereducing bacteria could play a significant role in vivianite formation in natural environments. Despite a low sulfate concentration (<20 µM), Lake Pavin hosts a plethora of sulfate-reducing bacteria in its water column (Lehours et al, 2005;Berg et al, 2019;Berg et al, 2020) and pyrite was found abundantly in the first 12 cm of its sediments, in association with abundant vivianite (Viollier et al, 1997;Busigny et al, 2014;Busigny et al, 2016). Although pyrite was only detected in the sediments and not in the water column, sulfate-rich enrichment cultures from this lake led to rapid pyrite formation after 21 days of culture (Berg et al, 2020).…”

“…Several studies of sulfate-reducing bacteria enrichments reported the formation of mackinawite (FeS) and greigite (Fe 3 S 4 ), both being potential precursors of pyrite (Fortin et al, 1994;Herbert et al, 1998;Watson et al, 2000;Gramp et al, 2009). Pyrites were obtained in some enrichments (Donald and Southam, 1999;Thiel et al, 2019;Berg et al, 2020), supporting the role of biology in sedimentary pyrite formation. However, due to the huge diversity of bacteria in these enrichments, especially iron-and sulfur-cycling bacteria (Lehours et al, 2009;Sitte et al, 2013;Zeng et al, 2018;Berg et al, 2019), deciphering the specific role of sulfate-reducing bacteria is tricky.…”

“…Pyrite formation through a greigite pathway has been suggested based on the occurrence of sedimentary magnetic pyrites and has been well studied Benning et al, 2000;Hunger and Benning, 2007;Lan and Butler, 2014). Although structurally complex (Rickard and Luther, 2007), the conversion of greigite to pyrite through a solid-state reaction may still be possible, as shown by hydrothermal experiments (Hunger and Benning, 2007) and, more recently, by the co-occurrence of greigite and nanocrystalline pyrite domains in micrometer-large pyrite spheres formed in an sulfate-reducing bacteria enrichment culture (Berg et al, 2020). Pyrite could thus have been produced by the reaction of greigite with zero-valent sulfur as follows:…”

“…Despite a low sulfate concentration (<20 µM), Lake Pavin hosts a plethora of sulfate-reducing bacteria in its water column (Lehours et al, 2005;Berg et al, 2019;Berg et al, 2020) and pyrite was found abundantly in the first 12 cm of its sediments, in association with abundant vivianite (Viollier et al, 1997;Busigny et al, 2014;Busigny et al, 2016). Although pyrite was only detected in the sediments and not in the water column, sulfate-rich enrichment cultures from this lake led to rapid pyrite formation after 21 days of culture (Berg et al, 2020). Here, our results demonstrate that the sole activity of Desulfovibrio (representing 80 % of the microbial consortium in the enrichment (Berg et al, 2020)) was able to promote pyrite formation.…”