Abstract
Abstract. To explore the potential role of tetrathionate in the sedimentary sulfur cycle, population ecology of microorganisms capable of metabolizing this polythionate was revealed at 15–30 cm resolution along two, ∼3 m long, cores collected from 530 and 580 m below the sea level, off India's west coast, within the oxygen minimum zone (OMZ) of the Arabian Sea. Metagenome analysis along the cores revealed widespread occurrence of genes involved in the formation, oxidation, and reduction of tetrathionate; high diversity and relative abundance were also detected for bacteria that are known to render these metabolisms in vitro. Results of slurry culture of the sediment samples in thiosulfate- or tetrathionate-containing microbial growth media, data obtained via pure-culture isolation, and finally metatranscriptome analyses corroborated the in situ functionality of the tetrathionate-forming, tetrathionate-oxidizing, and tetrathionate-reducing microorganisms. Ion chromatography of pore waters revealed the presence of up to 11.1 µM thiosulfate in the two cores, whereas tetrathionate remained undetected in spectroscopic assay based on its reaction with cyanide. While thiosulfate oxidation by chemolithotrophic bacteria prevalent in situ is the apparent source of tetrathionate in this ecosystem, high biochemical and geochemical reactivity of this polythionate could be instrumental in its cryptic status in the sulfur cycle. Potential abiotic origin of tetrathionate in the sediment horizon explored could neither be ruled out nor confirmed from the geochemical information available. On the other hand, tetrathionate potentially present in the system can be either oxidized to sulfate or reduced back to thiosulfate/sulfide via chemolithotrophic oxidation and respiration by native bacterial populations, respectively. Up to 2.01 mM sulfide present in the sediment cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. However, in the absence of measured data for O2 or other oxyanions having possibilities of serving as electron acceptors, the biogeochemical modalities of the oxidative half of the tetrathionate cycle remained unresolved.
Highlights
Diverse microorganisms oxidize or reduce different sulfur species to meet their bioenergetic requirements and in doing so play profound roles in biogeochemical sulfur cycling in nature (Baumgartner et al, 2006; Ghosh and Dam, 2009; Wasmund et al, 2017)
The tetrathionate formation-related genes identified included those encoding for the different subunits of the thiosulfate dehydrogenases TsdA (Denkmann et al, 2012; Pyne et al, 2018) and DoxDA (Quatrini et al, 2009), which catalyze the oxidation of thiosulfate to tetrathionate in taxonomically diverse bacteria and archaea
Concurrent with the above findings, direct taxonomic annotation of the raw metagenomic sequence datasets revealed that considerable proportions of the reads obtained for the individual sediment depths of SSK42/5 and SSK42/6 were ascribable to bacterial genera whose members are known to render tetrathionate formation, oxidation, or reduction
Summary
Diverse microorganisms oxidize or reduce different sulfur species to meet their bioenergetic requirements and in doing so play profound roles in biogeochemical sulfur cycling in nature (Baumgartner et al, 2006; Ghosh and Dam, 2009; Wasmund et al, 2017). There have been extensive studies of the benthic–sedimentary sulfur cycle across the global ocean (Jørgensen, 1990; Jørgensen and Bak, 1991; Rudnicki et al, 2001; Tostevin et al, 2014), and the focus of such investigations has typically been on geomicrobial transformations of Published by Copernicus Publications on behalf of the European Geosciences Union. Elemental sulfur and thiosulfate have been envisaged as constituting key junctions in the network of sulfur species transformations in the marine sediments (Jørgensen, 1990; Jørgensen and Bak, 1991; Thamdrup et al, 1994). Tetrathionate or other polythionates are rarely appreciated for their potential role(s) in marine sedimentary sulfur cycle, presumably because these sulfur species are not abundant in these environments
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