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.
All organisms possess fundamental metabolic pathways to ensure that needed carbon and sulfur compounds are provided to the cell in the proper chemical form and oxidation state. For most organisms capable of using CO2 as sole source of carbon, ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) catalyzes primary carbon dioxide assimilation. In addition, sulfur salvage pathways are necessary to ensure that key sulfur-containing compounds are both available and, where necessary, detoxified in the cell. Using knock-out mutations and metabolomics in the bacterium Rhodospirillum rubrum, we show here that Rubisco concurrently catalyzes key and essential reactions for seemingly unrelated but physiologically essential central carbon and sulfur salvage metabolic pathways of the cell. In this study, complementation and mutagenesis studies indicated that representatives of all known extant functional Rubisco forms found in nature are capable of simultaneously catalyzing reactions required for both CO2-dependent growth as well as growth using 5-methylthioadenosine as sole sulfur source under anaerobic photosynthetic conditions. Moreover, specific inactivation of the CO2 fixation reaction did not affect the ability of Rubisco to support anaerobic 5-methylthioadenosine metabolism, suggesting that the active site of Rubisco has evolved to ensure that this enzyme maintains both key functions. Thus, despite the coevolution of both functions, the active site of this protein may be differentially modified to affect only one of its key functions.
From the Department of Microbiology, The Ohio State University, Columbus, Ohio 43210 and.
Swati
S
Dey
From the Department of Microbiology, The Ohio State University, Columbus, Ohio 43210 and.
Justin A
JA
North
From the Department of Microbiology, The Ohio State University, Columbus, Ohio 43210 and.
Jaya
J
Sriram
the Donald Danforth Plant Science Center, St. Louis, Missouri, 63132.
Bradley S
BS
Evans
From the Department of Microbiology, The Ohio State University, Columbus, Ohio 43210 and tabita.1@osu.edu.
F Robert
http://orcid.org/0000-0001-7338-447X
FR
Tabita
D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D055162:Biocatalysis; D002244:Carbon / Q000378:metabolism; D002245:Carbon Dioxide / Q000378:metabolism*; D003839:Deoxyadenosines / Q000378:metabolism*; D053858:Metabolic Networks and Pathways; D012247:Rhodospirillum rubrum / Q000737:chemistry / Q000201:enzymology* / Q000235:genetics; D012273:Ribulose-Bisphosphate Carboxylase / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*; D013455:Sulfur / Q000378:metabolism; D013872:Thionucleosides / Q000378:metabolism*
D001426:Bacterial Proteins; D003839:Deoxyadenosines; D013872:Thionucleosides; D002245:Carbon Dioxide; C008500:5'-methylthioadenosine; D013455:Sulfur; D002244:Carbon; D012273:Ribulose-Bisphosphate Carboxylase
5-methylthioadenosine; carbon fixation; enzyme; metabolism; metabololomics; metabolomics; methylthioadenosine; ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO); sulfur; sulfur salvage