Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

Abstract

Summary Many questions regarding proteins involved in microbial sulfur metabolism remain unsolved. For sulfur respiration at low pH, the terminal electron acceptor is still unclear. Desulfurella amilsii is a sulfur‐reducing bacterium that respires elemental sulfur (S 0 ) or thiosulfate, and grows by S 0 disproportionation. Due to its versatility, comparative studies on D. amilsii may shed light on microbial sulfur metabolism. Requirement of physical contact between cells and S 0 was analyzed. Sulfide production decreased by around 50% when S 0 was trapped in dialysis membranes, suggesting that contact between cells and S 0 is beneficial, but not strictly needed. Proteome analysis was performed under the aforementioned conditions. A Mo‐oxidoreductase suggested from genome analysis to act as sulfur reductase was not detected in any growth condition. Thiosulfate and sulfite reductases showed increased abundance in thiosulfate‐reducing cultures, while rhodanese‐like sulfurtransferases were highly abundant in all conditions. DsrE and DsrL were abundantly detected during thiosulfate reduction, suggesting a modified mechanism of sulfite reduction. Proteogenomics suggest a different disproportionation pathway from what has been reported. This work points to an important role of rhodaneses in sulfur processes and these proteins should be considered in searches for sulfur metabolism in broader fields like meta‐omics.

The Iron-Sulfur Flavoprotein DsrL as NAD(P)H:Acceptor Oxidoreductase in Oxidative and Reductive Dissimilatory Sulfur Metabolism

“…In addition, DsrL is neither present in any of the filamentous cable bacteria, e.g., from the candidate genera Electrothrix and Electronema (Risgaard-Petersen et al, 2015;Trojan et al, 2016;Kjeldsen et al, 2019;Müller et al, 2019) nor in sulfide-oxidizing Desulfurivibrio species that cannot be distinguished from canonical sulfate-reducing bacteria using gene synteny or other genomic features (Thorup et al, 2017). On the other hand, the presence of dsrL in Desulfurella amilsii, an organism described as sulfur and thiosulfate reducer with the additional capacity for sulfur disproportionation, and in Candidatus Acididesulfobacter and Candidatus Acidulodesulfobacterium species that have been proposed to be capable of both sulfate reduction as well as sulfide oxidation has been noted and discussed earlier (Florentino et al, 2019;Tan et al, 2019), while its occurrence in a number of unclassified deltaproteobacterial metagenomes and metagenomes assigned to the families Desulfobacteraceae and Desulfobulbaceae has not attracted attention so far.…”

“…The latter is present in the vast majority of sulfur oxidizer genomes and indeed it has a documented essential function during sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum ( Lübbe et al, 2006 ). However, recent sequencing of genomes and metagenomes ( Florentino et al, 2017 , 2019 ; Anantharaman et al, 2018 ; Hausmann et al, 2018 ) as well as earlier sequencing of large environmental DNA fragments ( Mussmann et al, 2005 ), uncovered the presence of dsrL- related sequences also in a number of sulfate-, sulfite-, thiosulfate and/or sulfur-reducing as well as sulfur-disproportionating prokaryotes or in metagenomes encoding reductive-type DsrAB. DsrL forms a complex with rDsrAB in A. vinosum and biochemical data point at an in vivo function of the complex as a NAD(P)H:sulfite oxidoreductase with the DsrC protein acting as a co-substrate ( Löffler et al, 2020 ).…”

Genomic Characterization and Environmental Distribution of a Thermophilic Anaerobe Dissulfurirhabdus thermomarina SH388T Involved in Disproportionation of Sulfur Compounds in Shallow Sea Hydrothermal Vents

“…Finally, Mardanov et al (2016) [18] showed that direct cellular contact with sulfur is not required. As suggested in Florentino et al (2019) [19], certain molecular strategies could be involved in the assimilation of sulfur in cells, such as the formation of sulfur nanoparticles that can penetrate membranes, the nucleophilic attack of sulfur by sulfides that could generate polysulfides, used as a source of energy, or strategies involving flagella or pili.…”

“…Pathways of the disproportionation of sulfur are unknown and different pathways are very likely to exist. Some hypotheses have been proposed, such as the use of the complete or partial dissimilatory sulfate reduction pathway (adenylylsulfate reductase, heterodisulfide reductase, dissimilatory sulfite reductase), or the involvement of rhodanese-like sulfurtransferase or molybdopterins [ 18 , 19 , 20 ]. As suggested by Ward et al (2020) [ 21 ], a truncated AprB protein may also be involved in this process but this modified protein does not appear to be common in all sulfur disproportionators.…”

Long Chain Fatty Acid Degradation Coupled to Biological Sulfidogenesis: A Prospect for Enhanced Metal Recovery

“…The sulfide formed leaves the cell, while the sulfite enters the cytoplasm and gets reduced to sulfide. Overall, one sulfide is generated during the first step, directly from thiosulfate molecule, and the other is generated in the second step, during sulfite reduction (Surkov et al, 2000;Stoffels et al, 2012;Florentino et al, 2019).…”