Two pathways for thiosulfate oxidation in the alphaproteobacterial chemolithotrophParacoccus thiocyanatusSST

Abstract

Chemolithotrophic bacteria oxidize various sulfur species for energy and electrons, thereby operationalizing biogeochemical sulfur cycles in nature. The best-studied pathway of bacterial 25 sulfur-chemolithotrophy, involving direct oxidation of thiosulfate to sulfate (without any free intermediate) by the SoxXAYZBCD multienzyme system, is apparently the exclusive mechanism of thiosulfate oxidation in facultatively chemolithotrophic alphaproteobacteria. Here we explore the molecular mechanisms of sulfur oxidation in the thiosulfate-and tetrathionate-oxidizing alphaproteobacterium Paracoccus thiocyanatus SST, and compare them with the prototypical Sox 30 process characterized in Paracoccus pantotrophus. Our results revealed the unique case where, an alphaproteobacterium has Sox as its secondary pathway of thiosulfate oxidation, converting ~10% of the thiosulfate supplied whilst 90% of the substrate is oxidized via a Tetrathionate-Intermediate pathway. Knock-out mutation, followed by the study of sulfur oxidation kinetics, showed that thiosulfate-to-tetrathionate conversion, in SST, is catalyzed by a thiosulfate 35 dehydrogenase (TsdA) homolog that has far-higher substrate-affinity than the Sox system of this bacterium, which, remarkably, is also less efficient than the P. pantotrophus Sox. soxB-deletion in SST abolished sulfate-formation from thiosulfate/tetrathionate while thiosulfate-to-tetrathionate conversion remained unperturbed. Physiological studies revealed the involvement of glutathione in

Molecular mechanism of sulfur chemolithotrophy in the betaproteobacterium Pusillimonas ginsengisoli SBSA

“…As of now, based on the inability of the Pg_KoT to convert thiosulfate to tetrathionate, it can be assumed that the novel protein(s) involved in glutathione-tetrathionate coupling in SBSA, is not a dual-functional protein like ThdT. In this context, it is noteworthy that the involvement of glutathione and soxB (but not any ThdT homologue) in tetrathionate oxidation has recently been reported in the facultative chemolithotrophic alphaproteobacterium Paracoccus thiocyanatus SST [45]. These apparently novel tetrathionate-oxidizing (via glutathione conjugation) enzyme components might answer the long-open question of the molecular basis of tetrathionate oxidation outside the Acidithiobacillia group.…”

“…This nonfunctional status of their sox genes (in thiosulfate oxidation) could have stemmed from the presence of their alternative means for thiosulfate oxidation via the S 4 I pathway. Furthermore, it is also noteworthy that thiosulfate dehydrogenation that is apparently coded by two genes (tsdB and tsdA) has an obvious advantage over the Sox mechanism (coded by eight genes; soxCDYZAXOB) with respect to both horizontal gene transfer-mediated gain or loss of function via random mutagenesis, even though the co-existence and tandem function of a complete S 4 I pathway and Sox pathway is possible, as described in P. thiocyanatus SST [45]. The nonfunctional status of soxXAYZ and the loss of many otherwise-conserved residues in the sequence of corresponding proteins indicate a higher mutation rate in these four genes in the betaproteobacterial member P. ginsengisoli SBSA as well as in A. kashmirensis (see Fig S2-S5).…”

Aerobic microbial communities in the sediments of a marine oxygen minimum zone

“… 2013 ); the assay results were validated by ion chromatography (Rameez et al . 2020 ). New isolates were classified up to the lowest taxonomic category identifiable, using methods described by Saha et al .…”

A biochemical view on the biological sulfur cycle

“…The name "S 4 I" (S 4 intermediate) has been coined for the latter pathway which occurs in many beta-and gammaproteobacterial chemolithotrophs, e.g. species of the genus Acidithiobacillus (Bugaytsova & Lindström, 2004;Dam et al, 2007;Kikumoto et al, 2013;Pyne et al, 2017Pyne et al, , 2018Rameez et al, 2019;Visser et al, 1996). Two different enzymes initiating tetrathionate degradation have so far been described.…”