Cytoplasmic sulfur trafficking in sulfur‐oxidizing prokaryotes

Dahl, Christiane

doi:10.1002/iub.1371

Cited by 48 publications

(48 citation statements)

References 44 publications

(107 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A protein related to DsrE (DESAMIL20_1428), which is a sulfurtransferase in sulfur oxidizers (Dahl, ) was highly abundant exclusively in D. amilsii cultures growing by thiosulfate respiration (Fig. ), supporting its involvement in sulfite reduction.…”

Section: Resultsmentioning

confidence: 87%

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

Florentino

Pereira

Boeren

et al. 2018

Environmental Microbiology

View full text Add to dashboard Cite

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.

show abstract

Section: Resultsmentioning

confidence: 87%

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

Florentino

Pereira

Boeren

et al. 2018

Environmental Microbiology

View full text Add to dashboard Cite

show abstract

“…While a portion of these organisms employs the cytoplasmic Dsr pathway involving dissimilatory sulfite reductase [20], the central sulfur oxidation route is largely unknown for a huge array of other sulfur oxidizers including environmentally and biotechnologically highly relevant organisms like ore-leaching Acidithiobacillus species or thermoacidophilic archaea [17]. Metabolic reconstruction supported by microarray transcript profiling or comparative proteomics predicted the involvement of a heterodisulfide reductase-like HdrC1B1AHypHdrC2B2 complex in these organisms [17,[21][22][23] (Fig. 1) bearing resemblance to HdrABC from methanogens [24], although no coenzyme M-coenzyme B (CoM-S-S-CoB) heterodisulfide is present in the sulfur oxidizers.…”

Section: Introductionmentioning

confidence: 99%

A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds

Koch

Dahl

2018

The ISME Journal

Self Cite

View full text Add to dashboard Cite

Dimethylsulfide (DMS) plays a globally significant role in carbon and sulfur cycling and impacts Earth's climate because its oxidation products serve as nuclei for cloud formation. While the initial steps of aerobic DMS degradation and the fate of its carbon atoms are reasonably well documented, oxidation of the contained sulfur is largely unexplored. Here, we identified a novel pathway of sulfur compound oxidation in the ubiquitously occurring DMS-degrader Hyphomicrobium denitrificans X that links the oxidation of the volatile organosulfur compound with that of the inorganic sulfur compound thiosulfate. DMS is first transformed to methanethiol from which sulfide is released and fully oxidized to sulfate. Comparative proteomics indicated thiosulfate as an intermediate of this pathway and pointed at a heterodisulfide reductase (Hdr)-like system acting as a sulfur-oxidizing entity. Indeed, marker exchange mutagenesis of hdr-like genes disrupted the ability of H. denitrificans to metabolize DMS and also prevented formation of sulfate from thiosulfate provided as an additional electron source during chemoorganoheterotrophic growth. Complementation with the hdr-like genes under a constitutive promoter rescued the phenotype on thiosulfate as well as on DMS. The production of sulfate from an organosulfur precursor via the Hdr-like system is previously undocumented and provides a new shunt in the biogeochemical sulfur cycle. Furthermore, our findings fill a long-standing knowledge gap in microbial dissimilatory sulfur metabolism because the Hdr-like pathway is abundant not only in chemoheterotrophs, but also in a wide range of chemo- and photolithoautotrophic sulfur oxidizers acting as key players in global sulfur cycling.

show abstract

“…Fourteen proteins were more abundant in wild-type T. crunogena grown under DIC-limited conditions, with log 2 abundance ratios of Ͼ2 in both replicates of the proteome and q values of Ͻ0.05 (Table 1; see also Table S2 in the supplemental material). These include carboxysome shell proteins as well as carboxysomal enzymes RubisCO and carbonic anhydrase (encoded by Tcr_0838 to Tcr_0842), as anticipated given the role of carboxysomes in CCMs (as (23). Fourteen proteins were also upregulated in cells cultivated under high-DIC, NH 3 -limited conditions (Table 2).…”

Section: Resultsmentioning

confidence: 69%

Proteomic and Mutant Analysis of the CO ₂ Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena

et al. 2017

View full text Add to dashboard Cite

Many autotrophic microorganisms are likely to adapt to scarcity in dissolved inorganic carbon (DIC; CO 2 ϩ HCO 3 Ϫ ϩ CO 3 2Ϫ ) with CO 2 concentrating mechanisms (CCM) that actively transport DIC across the cell membrane to facilitate carbon fixation. Surprisingly, DIC transport has been well studied among cyanobacteria and microalgae only. The deep-sea vent gammaproteobacterial chemolithoautotroph Thiomicrospira crunogena has a low-DIC inducible CCM, though the mechanism for uptake is unclear, as homologs to cyanobacterial transporters are absent. To identify the components of this CCM, proteomes of T. crunogena cultivated under low-and high-DIC conditions were compared. Fourteen proteins, including those comprising carboxysomes, were at least 4-fold more abundant under low-DIC conditions. One of these proteins was encoded by Tcr_0854; strains carrying mutated copies of this gene, as well as the adjacent Tcr_0853, required elevated DIC for growth. Strains carrying mutated copies of Tcr_0853 and Tcr_0854 overexpressed carboxysomes and had diminished ability to accumulate intracellular DIC. Based on reverse transcription (RT)-PCR, Tcr_0853 and Tcr_0854 were cotranscribed and upregulated under low-DIC conditions. The Tcr_0853-encoded protein was predicted to have 13 transmembrane helices. Given the mutant phenotypes described above, Tcr_0853 and Tcr_0854 may encode a two-subunit DIC transporter that belongs to a previously undescribed transporter family, though it is widespread among autotrophs from multiple phyla.IMPORTANCE DIC uptake and fixation by autotrophs are the primary input of inorganic carbon into the biosphere. The mechanism for dissolved inorganic carbon uptake has been characterized only for cyanobacteria despite the importance of DIC uptake by autotrophic microorganisms from many phyla among the Bacteria and Archaea. In this work, proteins necessary for dissolved inorganic carbon utilization in the deep-sea vent chemolithoautotroph T. crunogena were identified, and two of these may be able to form a novel transporter. Homologs of these proteins are present in 14 phyla in Bacteria and also in one phylum of Archaea, the Euryarchaeota. Many organisms carrying these homologs are autotrophs, suggesting a role in facilitating dissolved inorganic carbon uptake and fixation well beyond the genus Thiomicrospira.KEYWORDS autotroph, bicarbonate transporter, carbon concentrating mechanism, carbon fixation, chemolithoautotroph, hydrothermal vent

show abstract

Cytoplasmic sulfur trafficking in sulfur‐oxidizing prokaryotes

Cited by 48 publications

References 44 publications

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds

Proteomic and Mutant Analysis of the CO ₂ Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena

Contact Info

Product

Resources

About

Cytoplasmic sulfur trafficking in sulfur‐oxidizing prokaryotes

Cited by 48 publications

References 44 publications

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

Insight into the sulfur metabolism of Desulfurella amilsii by differential proteomics

A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds

Proteomic and Mutant Analysis of the CO 2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena

Contact Info

Product

Resources

About

Proteomic and Mutant Analysis of the CO ₂ Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena