The oxidation of stored sulfur in phototrophic sulfur bacteria
Final Report Abstract
Reduced sulfur compounds such as sulfide and thiosulfate are oxidized by a large and diverse group of prokaryotes, including the phototrophic sulfur bacteria, the thiobacilli and other chemotrophic sulfur bacteria and some thermophilic archaea. Many of these organisms employ a pathway that includes the formation of zero-valent sulfur as a characteristic intermediate. In the purple sulfur bacterium and model organism Allochromatium vinosum sulfur globules are stored in the periplasmic space, a feature shared not only with a large number of environmentally important free-living chemotrophic sulfur oxidizers like Beggiatoa, Thioploca or magnetotactic bacteria but also with sulfur-oxidizing bacterial symbionts of marine animals like Riftia pachyptila or Olavius algarvensis. The complex degradation of sulfur stored in sulfur globules to sulfite is one of the least understood pathways in oxidative sulfur metabolism as it includes steps for activation and transport from the periplasm to the cytoplasm and requires the presence of many different enzymes encoded in the dsr operon including a reversely operating sulfite reductase (DsrAB). The dsr genes are not only found in sulfur-oxidizers but also in sulfate- and sulfite-reducing bacteria and archaea although the arrangement and composition of the Dsr proteins differs between sulfate-reducing organisms and sulfur oxidizers. The product of the Dsr pathway is sulfite, which is either directly oxidized to sulfate or indirectly via the intermediate adenylylsulfate (APS). In the course of the project reported about here, important purple bacterial Dsr proteins were characterized in detail with regard to their three-dimensional structure as well as their biochemical and biophysical properties. In addition, mutant strain analyses allowed insights into the in vivo functions of the proteins. A model for the Dsr pathway was developed that includes sulfur transfer to reverse-acting dissimilatory sulfite reductase via the sulfurtransferase DsrEFH and the subrstrate-binding protein DsrC. Sulfite and disulfidic oxidized DsrC are the products of the DsrAB-catalyzed reaction. DsrC is regenerated for the next reaction cycle by reduction via the membrane-bound DsrMKJOP complex. A function could as yet not be assigned to the essential DsrL protein. Studies on regulation of the dsr genes revealed that these are consitutively transcribed on a low level. Transcription is significantly increased in the presence of reduced sulfur compounds. One of the most surprising findings of our study was the observation that DsrC has a second function as a regulatory DNA-binding protein. furthermore, we collected data pointing at a regulatory function of DsrR and DsrS, both of which appear to be involved in post-transcriptional control of the dsr operon.
Publications
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(2008) Allochromatium vinosum DsrC: solution-state NMR structure, redox properties and interaction with DsrEFH, a protein essential for purple sulfur bacterial sulfur oxidation. J. Mol. Biol. 382, 692-707
Cort, J. R., Selan, U. M., Schulte, A., Grimm, F., Kennedy, M. A. & Dahl C.
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(2008) Inorganic sulfur compounds as electron donors in phototrophic sulfur bacteria. In Advances in photosynthesis and respiration (Govindjee, series editor), Vol. 27: Sulfur metabolism in phototrophic organisms (Hell, R., Dahl, C., Knaff, D. & Leustek, T., eds.) Springer, Dordrecht, 289-317
Dahl, C.
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(2008). Structural and molecular genetic insight into a wide-spread bacterial sulfur oxidation pathway. J. Mol. Biol. 384, 1287-1300
Dahl, C., Schulte, A., Stockdreher, Y., Hong, C., Grimm, F., Sander, J., Kim, R., Kim, S.-H. & Shin, D. H.
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(2009) Sulfur metabolism in phototrophic sulfur bacteria. Adv. Microb. Physiol. 54, 103-200
Frigaard, N. U. & Dahl, C.
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(2010) DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c. Biochemistry 49, 8290-8299
Grein, F., Venceslau, S. S., Schneider, L., Hildebrandt, P., Todorovic, S., Pereira, I.A.C. & Dahl, C.
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(2010) DsrR, a novel IscA-like protein lacking iron and Fe-S-binding function involved in the regulation of sulfur oxidation in Allochromatium vinosum. J. Bacteriol. 192, 1652-1661
Grimm, F., Cort, J. R. & Dahl, C.
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(2010) Regulation of dsr genes encoding proteins responsible for the oxidation of stored sulfur in Allochromatium vinosum. Microbiology 156, 764- 773
Grimm, F., Dobler, N. & Dahl, C.
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(2010) The Allochromatium vinsosum DsrMKJOP transmembrane complex: biochemical characterization of individual components aids understanding of complex function in vivo. J. Bacteriol. 192, 6369-6377
Grein, F., Pereira, I.A.C. & Dahl, C.
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(2011) Regulation of dissimilatory sulfur oxidation in the purple sulfur bacterium Allochromatium vinosum. Front. Microbio. 2, 51
Grimm, F., Franz, B. & Dahl, C.
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(2012) Cytoplasmic sulfurtransferases in the purple sulfur bacterium Allochromatium vinosum: Evidence for sulfur transfer from DsrEFH to DsrC. PLoS ONE 7, e40785
Stockdreher, Y., Venceslau, S. S., Josten, M., Sahl, H.-G., Pereira, I.A.C., & Dahl, C.
