Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators

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, similar to 3m long, cores collected from 530 and 580m 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 meta-transcriptome 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 mu M 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 2.01mM sulfide present in the sediment cores may also reduce tetrathionate abiotically to thiosulfate and elemental sulfur. However, in the absence of measured data for O-2 or other oxyanions having possibilities of serving as electron acceptors, the biogeochemical modalities of the oxidative half of the tetrathionate cycle remained unresolved.