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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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Autores principales: Claassens, Nico J., Scarinci, Giovanni, Fischer, Axel, Flamholz, Avi I., Newell, William, Frielingsdorf, Stefan, Lenz, Oliver, Bar-Even, Arren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7486775/
https://www.ncbi.nlm.nih.gov/pubmed/32820073
http://dx.doi.org/10.1073/pnas.2012288117
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author Claassens, Nico J.
Scarinci, Giovanni
Fischer, Axel
Flamholz, Avi I.
Newell, William
Frielingsdorf, Stefan
Lenz, Oliver
Bar-Even, Arren
author_facet Claassens, Nico J.
Scarinci, Giovanni
Fischer, Axel
Flamholz, Avi I.
Newell, William
Frielingsdorf, Stefan
Lenz, Oliver
Bar-Even, Arren
author_sort Claassens, Nico J.
collection PubMed
description 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 CO(2) concentrations, and testing autotrophic growth phenotypes of gene deletion strains at ambient CO(2). We find that the canonical plant-like C(2) 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 CO(2). 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.
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spelling pubmed-74867752020-09-23 Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle Claassens, Nico J. Scarinci, Giovanni Fischer, Axel Flamholz, Avi I. Newell, William Frielingsdorf, Stefan Lenz, Oliver Bar-Even, Arren Proc Natl Acad Sci U S A Biological Sciences 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 CO(2) concentrations, and testing autotrophic growth phenotypes of gene deletion strains at ambient CO(2). We find that the canonical plant-like C(2) 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 CO(2). 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. National Academy of Sciences 2020-09-08 2020-08-20 /pmc/articles/PMC7486775/ /pubmed/32820073 http://dx.doi.org/10.1073/pnas.2012288117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Claassens, Nico J.
Scarinci, Giovanni
Fischer, Axel
Flamholz, Avi I.
Newell, William
Frielingsdorf, Stefan
Lenz, Oliver
Bar-Even, Arren
Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title_full Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title_fullStr Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title_full_unstemmed Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title_short Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle
title_sort phosphoglycolate salvage in a chemolithoautotroph using the calvin cycle
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7486775/
https://www.ncbi.nlm.nih.gov/pubmed/32820073
http://dx.doi.org/10.1073/pnas.2012288117
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