In vivo studies in rhodospirillum rubrum indicate that ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) catalyzes two obligatorily required and physiologically significant reactions for distinct carbon and sulfur metabolic pathways

Journal of Biological Chemistry

Volumn 290, Issue 52, 2015, Pages 30658-30668

  Dey, Swati ^a   North, Justin A ^a   Sriram, Jaya ^a   Evans, Bradley S ^b   Tabita, F Robert ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CATALYSIS; CHEMICAL COMPOUNDS; METABOLISM; PHYSIOLOGY; SULFUR COMPOUNDS;

CHEMICAL FORMS; COMPLEMENTATION; METABOLIC PATHWAYS; OXIDATION STATE; RHODOSPIRILLUM RUBRUM; SALVAGE PATHWAY; SOLE SOURCE OF CARBON; SULFUR CONTAINING COMPOUND;

SULFUR;

5' METHYLTHIOADENOSINE; CARBON DIOXIDE; RIBULOSEBISPHOSPHATE CARBOXYLASE; 5'-METHYLTHIOADENOSINE; BACTERIAL PROTEIN; CARBON; DEOXYADENOSINE DERIVATIVE; NUCLEOSIDE; SULFUR;

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON METABOLISM; CARBON SOURCE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; IN VIVO STUDY; METABOLISM; METABOLOMICS; NONHUMAN; NUTRITION; PRIORITY JOURNAL; PROTEIN FUNCTION; RHODOSPIRILLUM RUBRUM; SULFUR METABOLISM; SULFUR SOURCE; BIOCATALYSIS; CHEMISTRY; ENZYMOLOGY; GENETICS;

BACTERIAL PROTEINS; BIOCATALYSIS; CARBON; CARBON DIOXIDE; DEOXYADENOSINES; METABOLIC NETWORKS AND PATHWAYS; RHODOSPIRILLUM RUBRUM; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SULFUR; THIONUCLEOSIDES;

EID: 84951748491     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.691295     Document Type: Article

References (36)

1. Cleland, W. W., Andrews, T. J., Gutteridge, S., Hartman, F. C., and Lorimer, G. H. (1998) Mechanism of RubisCO: The carbamate as general base. Chem. Rev. 98, 549-562
2. Spreitzer, R. J., and Salvucci, M. E. (2002) Rubisco: Structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol. 53, 449-475
3. Hauser, T., Popilka, L., Hartl, F. U., and Hayer-Hartl, M. (2015) Role of auxiliary proteins in Rubisco biogenesis and function. Nature Plants 1, 15065
4. Tabita, F. R. (1999) Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A different perspective. Photosynth. Res. 60, 1-28
5. Hanson, T. E., and Tabita, F. R. (2001) A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 98, 4397-4402
6. Tabita, F. R., Hanson, T. E., Li, H., Satagopan, S., Singh, J., and Chan, S. (2007) Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71, 576-599
7. Tabita, F. R., Hanson, T. E., Satagopan, S., Witte, B. H., and Kreel, N. E. (2008) Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Phil. Trans. R. Soc. Lond. B Biol. Sci. 363, 2629-2640
8. Li, H., Sawaya, M. R., Tabita, F. R., and Eisenberg, D. (2005) Crystal structure of a novel RuBisCO-like protein from the green sulfur bacterium Chlorobium tepidum. Structure 13, 779-789
9. Hanson, T. E., and Tabita, F. R. (2003) Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the RubisCO-like protein. Photosynth. Res. 78, 231-248
10. Ashida, H., Saito, Y., Kojima, C., Kobayashi, K., Ogasawara, N., and Yokota, A. (2003) A functional link between Rubisco-like protein of Bacillus and photosynthetic Rubisco. Science 302, 286-290
11. Carré-Mlouka, A., Méjean, A., Quillardet, P., Ashida, H., Saito, Y., Yokota, A., Callebaut, I., Sekowska, A., Dittmann, E., Bouchier, C., and de Marsac, N. T.(2006) A new RubisCO-like protein coexists with a photosynthetic Rubisco in the planktonic cyanobacteria Microcystis. J. Biol. Chem. 281, 24462-24471
12. Imker, H. J., Fedorov, A. A., Fedorov E. V., Almo, S. C., and Gerlt, J. A. (2007) Mechanistic diversity in the RuBisCO superfamily: The "enolase" in the methionine salvage pathway in Geobacillus kaustophilus. Biochemistry 46, 4077-4089
13. Erb, T. J., Evans, B. S., Cho, K., Warlick, B. P., Sriram, J., Wood, B. M., Imker, H. J., Sweedler, J. V., Tabita, F. R., and Gerlt, J. A. (2012) A RubisCO-like protein links SAM metabolism with isoprenoid biosynthesis. Nat. Chem. Biol. 8, 926-932
14. Singh, J., and Tabita, F. R. (2010) Role of RubisCO and the RubisCO-like protein in 5-methyladenosine metabolism in the nonsulfur bacterium Rhodospirillum rubrum. J. Bacteriol. 192, 1324-1331
15. Warlick, B. P., Imker, H. J., Sriram, J., Tabita, F. R., and Gerlt, J. A. (2012) Mechanistic Diversity in the RubisCO Superfamily: The RubisCO from Rhodospirillum rubrum is not promiscuous for reactions catalyzed by RubisCO-like proteins (RLPs). Biochemistry 51, 9470-9479
16. Munk, A. C., Copeland, A., Lucas, S., Lapidus, A., Del Rio, T. G., Barry, K., Detter, J. C., Hammon, N., Israni, S., Pitluck, S., Brettin, T., Bruce, D., Han, C., Tapia, R., Gilna, P., Schmutz, J., Larimer, F., Land, M., Kyrpides, N. C., Mavromatis, K., Richardson, P., Rohde, M., Göker, M., Klenk, H. P., Zhang, Y., Roberts, G. P., Reslewic, S., and Schwartz, D. C. (2011) Complete genome sequence of Rhodospirillum rubrum type strain (S1). Stand. Genomic Sci. 4, 293-302
17. Falcone, D. L., and Tabita, F. R. (1993) Complementation analysis and regulation of CO2 fixation gene expression in a ribulose-1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum. J. Bacteriol. 175, 5066-5077
18. Wang, D., Zhang, Y., Welch, E., Li, J., and Roberts, G. P. (2010) Elimination of RubisCO alters the regulation of nitrogenase activity and increases hydrogen production in Rhodospirillum rubrum. Int. J. Hydrogen Energy 35, 7377-7385
19. Smith, S. A., and Tabita, F. R. (2003) Positive and negative selection of mutant forms of prokaryotic (cyanobacterial) ribulose-1, 5-bisphosphate carboxylase/oxygenase. J. Mol. Biol. 331, 557-569
20. Satagopan, S., Scott, S. S., Smith, T. G., and Tabita, F. R. (2009) A RubisCO mutant that confers growth under a normally "inhibitory" oxygen concentration. Biochemistry 48, 9076-9083
21. Witte, B. H. (2012) Taming the Wild RubisCO: Explorations in Functional Metagenomics. Ph.D. thesis, The Ohio State University
22. Satagopan, S., Chan, S., Perry, L. J., and Tabita, F. R. (2014) Structurefunction studies with the unique hexameric form II ribulose-1,5-bisphosphate carboxylase/oxygenase (RubsiCO) from Rhodospeudomonas plaustris. J. Biol. Chem. 289, 21433-21450
23. Gibson, J. L., and Tabita, F. R. (1986) Isolation of the Rhodopseudomonas sphaeroides form I ribulose 1,5-bisphosphate carboxylase/oxygenase large and small subunit genes and expression of the active hexadecameric enzyme in Escherichia coli. Gene 44, 271-278
24. Ormerod, J. G., Ormerod, K. S., and Gest, H. (1961) Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism. Arch. Biochem. Biophys. 94, 449-463
25. Peleg, M., and Corradini, M. G. (2011) Microbial growth curves: What the models tell us and what they cannot. Crit. Rev. Food Sci. Nutr. 51, 917-945
26. Schlenk, F., and Ehninger, J. (1964) Observation of 5'-methylthioadenosine. Arch. Biochem. Biophys. 106, 95-100
27. Imker, H. J., Singh, J., Warlick B. P., Tabita, F. R., and Gerlt, J. A. (2008) Mechanistic diversity in the RubisCO superfamily: A novel isomerization reaction catalyzed by the Rubisco-like protein from Rhodospirillum rubrum. Biochemistry 47, 11171-11173
28. Joshi, H. M., and Tabita, F. R. (1996) A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc. Natl. Acad. Sci. U.S.A. 93, 14515-14520
29. McKinlay, J. B., and Harwood, C. S. (2010) Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc. Natl. Acad. Sci. U.S.A. 107, 11669-11675
30. Alonso, H., Blayney, M. J., Beck, J. L., and Whitney, S. M. (2009) Substrateinduced assembly of Methanococcoides burtonii D-ribulose-1,5-bisphosphate carboxylase/oxygenase dimers into decamers. J. Biol. Chem. 284, 33876-33882
31. Smith, S. A., and Tabita, F. R. (2004) Glycine 176 affects catalytic properties and stability of the Synechococcus sp. Strain PCC 6301 ribulose-1,5-bisphosphate carboxylase/oxygenase. J. Biol. Chem. 279, 25632-25637
32. Wang, D., Zhang, Y., Pohlmann, E. L., Li, J., and Roberts G. P. (2011) The poor growth of Rhodospirillum rubrum mutants lacking RubisCO is due to the accumulation of ribulose-1,5-bisphosphate. J. Bacteriol. 193, 3293-3303
33. Kim, K., and Portis, A. R., Jr. (2004) Oxygen-dependent H2O2 production by RubisCO. FEBS Lett. 571, 124-128
34. Rébeillé, F., Jabrin, S., Bligny, R., Loizeau, K., Gambonnet, B., Van Wilder, V., Douce, R., and Ravanel, S. (2006) Methionine catabolism in Arabidopsis cells is initiated by a γ-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc. Natl. Acad. Sci. U.S.A. 103, 15687-15692
35. Cipollone, R., Ascenzi, P., and Visca, P. (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59, 51-59
36. Chan, C. M., Danchin, A., Marlière, P., and Sekowska, A. (2014) Paralogous metabolism: S-alkyl-cysteine degradation in Bacillus subtilis. Environ. Microbiol. 16, 101-117