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Cueva de la Mora is a permanently stratified acidic pit lake with extremely high concentrations of heavy metals at depth. In order to evaluate the potential for in situ sulfide production, we characterized the microbial community in the deep layer using metagenomics and metatranscriptomics. We retrieved 18 high quality metagenome-assembled genomes (MAGs) representing the most abundant populations. None of the MAGs were closely related to either cultured or non-cultured organisms from the Genome Taxonomy or NCBI databases (none with average nucleotide identity >95%). Despite oxygen concentrations that are consistently below detection in the deep layer, some archaeal and bacterial MAGs mapped transcripts of genes for sulfide oxidation coupled with oxygen reduction. Among these microaerophilic sulfide oxidizers, mixotrophic Thermoplasmatales archaea were the most numerous and represented 24% of the total community. Populations associated with the highest predicted in situ activity for sulfate reduction were affiliated with Actinobacteria, Chloroflexi, and Nitrospirae phyla, and together represented about 9% of the total community. These MAGs, in addition to a less abundant Proteobacteria MAG in the genus Desulfomonile, contained transcripts of genes in the Wood-Ljungdahl pathway. All MAGs had significant genetic potential for organic carbon oxidation. Our results indicate that novel acidophiles are contributing to biosulfidogenesis in the deep layer of Cueva de la Mora, and that in situ sulfide production is limited by organic carbon availability and sulfur oxidation. 

Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S⁰) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen‐rich meteoric water, creating Proterozoic‐like conditions and supporting a prolific ecosystem driven by sulfur‐based chemolithoautotrophy. To better understand the cycling of S⁰in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide‐oxidizing mats dominated byBeggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related toSulfurovum,Halothiobacillus,Thiofaba,Thiovirga,Thiobacillus, andDesulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated withBacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae.DesulfocapsaandSulfurovumpopulations accounted for 12%–26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S⁰disproportionation in pure culture. Gibbs energy (∆G_r) calculations revealed that S⁰disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat‐sediment interface showed thatBeggiatoamats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S⁰generated by microbial sulfide oxidation in this oxygen‐limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur‐rich environments.

 

This work shines light on the role of extracellular polymeric substance (EPS) in the formation and preservation of elemental sulfur biominerals produced by sulfur-oxidizing bacteria. We characterized elemental sulfur particles produced within a Sulfurovum -rich biofilm in the Frasassi Cave System (Italy). The particles adopt spherical and bipyramidal morphologies, and display both stable (α-S 8 ) and metastable (β-S 8 ) crystal structures. Elemental sulfur is embedded within a dense matrix of EPS, and the particles are surrounded by organic envelopes rich in amide and carboxylic groups. Organic encapsulation and the presence of metastable crystal structures are consistent with elemental sulfur organomineralization, i.e., the formation and stabilization of elemental sulfur in the presence of organics, a mechanism that has previously been observed in laboratory studies. This research provides new evidence for the important role of microbial EPS in mineral formation in the environment. We hypothesize that the extracellular organics are used by sulfur-oxidizing bacteria for the stabilization of elemental sulfur minerals outside of the cell wall as a store of chemical energy. The stabilization of energy sources (in the form of a solid electron acceptor) in biofilms is a potential new role for microbial EPS that requires further investigation.