Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

Carbon fixation via the Calvin cycle is constrained by the side activity of Rubisco with dioxygen, generating 2-phosphoglycolate. The metabolic recycling of phosphoglycolate was extensively studied in photoautotrophic organisms, including plants, algae, and cyanobacteria, where it is referred to as...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2020-09, Vol.117 (36), p.22452-22461
Main Authors: Claassens, Nico J., Scarinci, Giovanni, Fischer, Axel, Flamholz, Avi I., Newell, William, Frielingsdorf, Stefan, Lenz, Oliver, Bar-Even, Arren
Format: Article
Language:English
Subjects:
Algae
Autotrophs
Bacteria
Biological Sciences
Calvin cycle
Carbon cycle
Carbon dioxide
Carbon fixation
Coenzyme A
Cyanobacteria
Decarboxylation
Gene deletion
Malate
Metabolism
Microorganisms
Phenotypes
Photorespiration
Recycling
Ribulose-bisphosphate carboxylase
Soil bacteria
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Summary:Carbon fixation via the Calvin cycle is constrained by the side activity of Rubisco with dioxygen, generating 2-phosphoglycolate. The metabolic recycling of phosphoglycolate was extensively studied in photoautotrophic organisms, including plants, algae, and cyanobacteria, where it is referred to as photorespiration. While receiving little attention so far, aerobic chemolithoautotrophic bacteria that operate the Calvin cycle independent of light must also recycle phosphoglycolate. As the term photorespiration is inappropriate for describing phosphoglycolate recycling in these nonphotosynthetic autotrophs, we suggest the more general term “phosphoglycolate salvage.” Here, we study phosphoglycolate salvage in the model chemolithoautotroph Cupriavidus necator H16 (Ralstonia eutropha H16) by characterizing the proxy process of glycolate metabolism, performing comparative transcriptomics of autotrophic growth under low and high CO₂ concentrations, and testing autotrophic growth phenotypes of gene deletion strains at ambient CO₂. We find that the canonical plant-like C₂ cycle does not operate in this bacterium, and instead, the bacterial-like glycerate pathway is the main route for phosphoglycolate salvage. Upon disruption of the glycerate pathway, we find that an oxidative pathway, which we term the malate cycle, supports phosphoglycolate salvage. In this cycle, glyoxylate is condensed with acetyl coenzyme A (acetyl-CoA) to give malate, which undergoes two oxidative decarboxylation steps to regenerate acetyl-CoA. When both pathways are disrupted, autotrophic growth is abolished at ambient CO₂. We present bioinformatic data suggesting that the malate cycle may support phosphoglycolate salvage in diverse chemolithoautotrophic bacteria. This study thus demonstrates a so far unknown phosphoglycolate salvage pathway, highlighting important diversity in microbial carbon fixation metabolism.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2012288117