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  Rubisco condensate formation by CcmM in beta-carboxysome biogenesis

Wang, H., Yan, X., Aigner, H., Bracher, A., Nguyen, N. D., Hee, W. Y., et al. (2019). Rubisco condensate formation by CcmM in beta-carboxysome biogenesis. Nature, 566(7742), 131-135. doi:10.1038/s41586-019-0880-5.

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Item Permalink: http://hdl.handle.net/21.11116/0000-0003-3F8F-7 Version Permalink: http://hdl.handle.net/21.11116/0000-0003-3F90-4
Genre: Journal Article

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 Creators:
Wang, H.1, Author              
Yan, X.1, Author              
Aigner, H.1, Author              
Bracher, A.1, Author              
Nguyen, N. D.2, Author
Hee, W. Y.2, Author
Long, B. M.2, Author
Price, G. D.2, Author
Hartl, F. U.1, Author              
Hayer-Hartl, M.3, Author              
Affiliations:
1Hartl, Franz-Ulrich / Cellular Biochemistry, Max Planck Institute of Biochemistry, Max Planck Society, ou_1565152              
2external, ou_persistent22              
3Hayer-Hartl, Manajit / Chaperonin-assisted Protein Folding, Max Planck Institute of Biochemistry, Max Planck Society, ou_1565153              

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Free keywords: LIQUID PHASE-SEPARATION; CARBONIC-ANHYDRASE; SYNECHOCOCCUS PCC7942; ASSEMBLY CHAPERONE; CO2 FIXATION; CYANOBACTERIUM; PHOTOSYNTHESIS; MECHANISM; GENES; EXPRESSIONScience & Technology - Other Topics;
 Abstract: Cells use compartmentalization of enzymes as a strategy to regulate metabolic pathways and increase their efficiency(1). The alpha- and beta-carboxysomes of cyanobacteria contain ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)-a complex of eight large (RbcL) and eight small (RbcS) subunits-and carbonic anhydrase(2-4). As HCO3- can diffuse through the proteinaceous carboxysome shell but CO2 cannot(5), carbonic anhydrase generates high concentrations of CO2 for carbon fixation by Rubisco(6). The shell also prevents access to reducing agents, generating an oxidizing environment(7-9). The formation of beta-carboxysomes involves the aggregation of Rubisco by the protein CcmM(10), which exists in two forms: full-length CcmM (M58 in Synechococcus elongatus PCC7942), which contains a carbonic anhydrase-like domain(8) followed by three Rubisco small subunit-like (SSUL) modules connected by flexible linkers; and M35, which lacks the carbonic anhydrase-like domain(11). It has long been speculated that the SSUL modules interact with Rubisco by replacing RbcS(2-4). Here we have reconstituted the Rubisco-CcmM complex and solved its structure. Contrary to expectation, the SSUL modules do not replace RbcS, but bind close to the equatorial region of Rubisco between RbcL dimers, linking Rubisco molecules and inducing phase separation into a liquid-like matrix. Disulfide bond formation in SSUL increases the network flexibility and is required for carboxysome function in vivo. Notably, the formation of the liquid-like condensate of Rubisco is mediated by dynamic interactions with the SSUL domains, rather than by low-complexity sequences, which typically mediate liquid-liquid phase separation in eukaryotes(12,13). Indeed, within the pyrenoids of eukaryotic algae, the functional homologues of carboxysomes, Rubisco adopts a liquid-like state by interacting with the intrinsically disordered protein EPYC1(14). Understanding carboxysome biogenesis will be important for efforts to engineer CO2-concentrating mechanisms in plants(15-19).

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Language(s): eng - English
 Dates: 2019
 Publication Status: Published in print
 Pages: 21
 Publishing info: -
 Table of Contents: We thank ... M. Strauss, J. Plitzko, F. Beck, S. Albert and Q. Guo (MPIB cryo-EM facility) for input on data collection and processing; ... and the staff at the MPIB Crystallization and Imaging facilities ...
 Rev. Method: -
 Identifiers: ISI: 000457981800052
DOI: 10.1038/s41586-019-0880-5
 Degree: -

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Project name : SFB1035
Grant ID : -
Funding program : -
Funding organization : Deutsche Forschungsgemeinschaft

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Title: Nature
  Abbreviation : Nature
Source Genre: Journal
 Creator(s):
Affiliations:
Publ. Info: London : Nature Publishing Group
Pages: - Volume / Issue: 566 (7742) Sequence Number: - Start / End Page: 131 - 135 Identifier: ISSN: 0028-0836
CoNE: https://pure.mpg.de/cone/journals/resource/954925427238