Sulfide oxidation forms a critical step in the global sulfur cycle, although this process is notoriously difficult to constrain due to the multiple pathways and highly reactive intermediates involved. Multiple sulfur isotopes (δ34S and δ33S) can provide a powerful tool for unravelling sulfur cycling processes in modern (and ancient) environments, although they have had limited application to systems with well-resolved oxidative S cycling. In this study, we report the major (δ34S) and minor (δ33S) isotope values of sulfur compounds in streams and sediments from the sulfidic Frasassi cave system, Marche Region, Italy. These microaerophilic cave streams host prominent white biofilms dominated by chemolithotrophic organisms that oxidize sulfide to S0, allowing us to estimate S isotope fractionations associated with in situ sulfide oxidation and to evaluate any resulting isotope biosignatures. Our results demonstrate that chemolithotrophic sulfide oxidation produces 34S enrichments in the S0 products that are larger than those previously measured in laboratory experiments, with 34εS0-H2S of up to 8‰ calculated. These small reverse isotope effects are similar to those produced during phototrophic sulfide oxidation (≤7‰), but distinct from the small normal isotope effects previously calculated for abiotic oxidation of sulfide with O2 (~-5‰). An inverse correlation between the magnitude of 34εS0-H2S effects and sulfide availability, along with substantial differences in δ33S, both support complex sulfide oxidation pathways and intracellular recycling of S intermediates by organisms inhabiting the biofilms. At the ecosystem level, we calculate fractionations of less than 40‰ between sulfide and sulfate in the water column and in the sediments. These fractionations are smaller than those typically calculated for systems dominated by sulfate reduction (> 50‰), and contrast with the commonly held assumption that oxidative recycling of sulfide generally increases overall fractionations. The relatively small fractionations appear to be related to the sequestration of S0 in the biofilms (either intra- or extra-cellularly), which removes this intermediate substrate from fractionation by further disproportionation or oxidation reactions. In addition, the net 33λH2S-SO4 values calculated in this system are larger than data published for systems dominated by reductive sulfur cycling, partially due to the isotopic imprint of chemolithotrophic sulfide oxidation on the aqueous sulfide pool. These distinct isotopic relationships are retained in the sedimentary sulfur pool, suggesting that trends in 34S and 33S values could provide an isotopic fingerprint of such chemolithotrophic ecosystems in modern and ancient environments.
Bibliographical noteFunding Information:
The authors thank A. Montanari for providing logistical support and the use of facilities and laboratory space at the Osservatorio Geologico di Coldigioco in Italy. Thanks to S. Mariani, S. Cerioni, M. Mainiero, F. Baldoni, S. Carnevali and members of the Gruppo Speleologico C.A.I. di Fabriano and Ancona for technical assistance during field campaigns, and to S. Dattagupta, R. McCauley, K. Dawson and C. Chan for assistance with sampling. We additionally thank Associated Editor D. Johnston and K. Mandernack for constructive reviews that greatly improved the manuscript. This work was supported by NASA Exobiology ( NNX07AV54G ) (A.Z. and J.F.), a Natural Environment Research Council Fellowship ( NE/H016805 ) (A.Z.), the National Science Foundation (NSF EAR-0525503 and EAR-1124411 ) (J.M.), and the NASA Astrobiology Institute (PSARC, NNA04CC06A ) (J.M.).
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