A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea

Kono, Takunari; Mehrotra, Santosh; Endo, Chikako; Kizu, Natsuko; Matusda, Mami; Kimura, Hiroyuki; Mizohata, Eiichi; Inoue, Tsuyoshi; Hasunuma, Tomohisa; Yokota, Akiho; Matsumura, Hideki; Ashida, Hiroshi

doi:10.1038/ncomms14007

Cited by 109 publications

(109 citation statements)

References 65 publications

(72 reference statements)

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“…These observations suggest deep links between carbon and sulphur metabolism. It is tempting to relate this observation to the discovery of a role of a class of RuBisCO protein in the ‘reductive hexulose‐phosphate pathway’ discovered in methanogenic archaea (Kono et al ., ). This pathway resembles the photosynthetic Calvin–Benson cycle.…”

Section: Alternate Fates Of Mtru‐1‐p and Its By‐productsmentioning

confidence: 97%

Revisiting the methionine salvage pathway and its paralogues

Sekowska

Ashida

Danchin

2018

Microbial Biotechnology

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SummaryMethionine is essential for life. Its chemistry makes it fragile in the presence of oxygen. Aerobic living organisms have selected a salvage pathway (the MSP) that uses dioxygen to regenerate methionine, associated to a ratchet‐like step that prevents methionine back degradation. Here, we describe the variation on this theme, developed across the tree of life. Oxygen appeared long after life had developed on Earth. The canonical MSP evolved from ancestors that used both predecessors of ribulose bisphosphate carboxylase oxygenase (RuBisCO) and methanethiol in intermediate steps. We document how these likely promiscuous pathways were also used to metabolize the omnipresent by‐products of S‐adenosylmethionine radical enzymes as well as the aromatic and isoprene skeleton of quinone electron acceptors.

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Section: Alternate Fates Of Mtru‐1‐p and Its By‐productsmentioning

confidence: 97%

Revisiting the methionine salvage pathway and its paralogues

Sekowska

Ashida

Danchin

2018

Microbial Biotechnology

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“…3) suggest that these Thaumarchaeota may be aerobic heterotrophs. The regeneration in the RHP pathway involves the activity of PRK, which the organism encodes (56). 210…”

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confidence: 99%

“…In these methanogens, the ribulose monophosphate (RuMP) pathway (involved in 211 methylotrophic formaldehyde assimilation and detoxification) is hypothesized to operate in 212 reverse, fixing CO2 via RuBisCO and PRK. A key intermediate, fructose-6-phosphate, is derived 213 from gluconeogenesis, which cyclizes the pathway (56). 214…”

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confidence: 99%

Aerobic heterotrophy and RuBisCO-mediated CO₂metabolism in marineThaumarchaeota

Reji

Francis

2019

Preprint

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1Thaumarchaeota constitute an abundant and ubiquitous phylum of Archaea that play critical 2 roles in the global nitrogen and carbon cycles. Most well-characterized members of the phylum 3 are chemolithoautotrophic ammonia-oxidizing archaea (AOA), which comprise up to 5 and 20 % 4 of the total single-celled life in soil and marine systems, respectively. Using two high-quality 5 metagenome-assembled genomes (MAGs), here we describe a divergent marine thaumarchaeal 6 clade that is devoid of the ammonia-oxidation machinery and the AOA-specific carbon-fixation 7 pathway. Phylogenomic analyses placed these genomes within the uncultivated and largely 8 understudied marine pSL12-like thaumarchaeal clade. The predominant mode of nutrient 9 acquisition appears to be aerobic heterotrophy, evidenced by the presence of respiratory 10 complexes and various organic carbon degradation pathways. Unexpectedly, both genomes 11 encoded a form III RuBisCO. Genomic composition of the MAGs is consistent with the role of 12RuBisCO in nucleotide salvage, as has been proposed previously for archaea harboring the form 13 III variant. Metabolic reconstructions revealed a complete nonoxidative pentose phosphate 14 pathway (PPP) and gluconeogenesis, which can cyclize the RuBisCO-mediated carbon metabolic 15 pathway. We conclude that these genomes represent a hitherto unrecognized evolutionary link 16 between predominantly anaerobic basal thaumarchaeal lineages and mesophilic marine AOA, 17 with important implications for diversification within the phylum Thaumarchaeota. 18

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“…S5). Our GAPDH-CP12 crystal structure together with a partial model of PRK from an archaeal homolog (13) was used as a basis for model building of the entire complex in Coot (14), and model refinement with Phenix (15) real space refine ( Fig.2B, table S2).…”

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Structural basis of light-induced redox regulation in the Calvin cycle

McFarlane

Shah

Kabasakal

et al. 2018

Preprint

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In plants, carbon dioxide is fixed via the Calvin cycle in a tightly regulated process. Key to this regulation is the conditionally disordered protein CP12. CP12 forms a complex with two Calvin cycle enzymes, glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and phosphoribulokinase (PRK), inhibiting their activities. The mode of CP12 action was unknown. By solving crystal structures of CP12 bound to GAPDH, and the ternary GAPDH-CP12-PRK complex by electron cryo-microscopy, we reveal that formation of the N-terminal disulfide pre-orders CP12 prior to binding the PRK active site. We find that CP12 binding to GAPDH influences substrate accessibility of all GAPDH active sites in the binary and ternary inhibited complexes. Our model explains how CP12 integrates responses from both redox state and nicotinamide dinucleotide availability to regulate carbon fixation. One Sentence Summary:How plants turn off carbon fixation in the dark.The Calvin cycle fixes organic carbon to provide fuel for plants, a process tightly controlled by light-induced redox changes in regulated enzymes (1). Phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) are essential enzymes in the photosynthetic dark reactions that control availability of substrate for the carboxylation enzyme Rubisco. PRK consumes ATP to produce the Rubisco substrate ribulose bisphosphate (RuBP), while GAPDH catalyses the reduction step of the Calvin cycle with NADPH to produce the sugar, glyceraldehyde 3-phosphate (GAP), which is used for regeneration of RuBP and is the main exit point of the cycle (2). GAPDH and PRK are coregulated in response to the light reactions, which produce ATP and NADPH. In the light, NADPH and reduced ferredoxin are produced in the chloroplast stroma and the two disulfides of PRK are reduced to switch on PRK activity (3). GAPDH has no disulfides, instead redox regulation of GAPDH is driven by two disulfide bonds in the small regulatory inhibitor protein CP12 (4, 5), which is disordered under reducing conditions (6). In the dark, the stroma becomes oxidizing and intramolecular disulfide bonds within PRK and CP12 are formed. CP12 binds and inhibits GAPDH and then PRK activity in an obligate sequential reaction (7). CP12 is present in oxygenic phototrophs from cyanobacteria to plants (8). Previous structural studies of the GAPDH-CP12 complex resolved only a C-terminal fragment of CP12, so it remained unclear how CP12 could regulate both enzymes. A recent structure of a cyanobacterial CP12-CBS protein resolved an N-terminal CP12-like region, however the protein does not form a ternary complex with GAPDH and PRK (9). The lack of

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A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea

Cited by 109 publications

References 65 publications

Revisiting the methionine salvage pathway and its paralogues

Revisiting the methionine salvage pathway and its paralogues

Aerobic heterotrophy and RuBisCO-mediated CO₂metabolism in marineThaumarchaeota

Structural basis of light-induced redox regulation in the Calvin cycle

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A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea

Cited by 109 publications

References 65 publications

Revisiting the methionine salvage pathway and its paralogues

Revisiting the methionine salvage pathway and its paralogues

Aerobic heterotrophy and RuBisCO-mediated CO2metabolism in marineThaumarchaeota

Structural basis of light-induced redox regulation in the Calvin cycle

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Aerobic heterotrophy and RuBisCO-mediated CO₂metabolism in marineThaumarchaeota