From CO2 to Cell: Energetic Expense of Creating Biomass Using the Calvin-Benson-Bassham and Reductive Citric Acid Cycles Based on Genomic Data

Abstract

Abstract The ubiquity of the Calvin-Benson-Bassham cycle (CBB) amongst autotrophic organisms suggests that it provides an advantage over a wide range of environmental conditions. However, in some habitats, such as hydrothermal vents, the reductive citric acid cycle (rCAC) is an equally predominant carbon fixation pathway. It has been suggested that the CBB cycle poses a disadvantage under certain circumstances due to being more energetically demanding compared to other carbon fixation pathways. The purpose of this study was to compare the relative metabolic cost of cell biosynthesis by an autotrophic cell using either the CBB cycle or the rCAC. For both pathways, the energy, in ATP, required to synthesize the macromolecules (DNA, RNA, protein, and cell envelope) for one gram of biomass was calculated, beginning with CO2. Two sulfur-oxidizing chemolithoautotrophic proteobacteria, Thiomicrospira crunogena XCL-2, and Sulfurimonas autotrophica were used to model the CBB cycle and rCAC, respectively while Escherichia coli was used to model both pathways because it has had its cell composition extremely well-characterized. Since these organisms have had their genomes sequenced, it was possible to reconstruct the biochemical pathways necessary for intermediate and macromolecule synthesis. Prior estimates, based solely on the ATP cost of pyruvate biosynthesis, suggested that the cellular energetic expense for biosynthesis from the CBB cycle was more than that from the rCAC. The results of this study support this conclusion; however the difference in expense between the two pathways may not be as extreme as suggested by pyruvate synthesis. Other factors, such as oxygen sensitivity, may act in concert with energetic expense in contributing to the selective advantages between different autotrophic carbon fixation pathways