Rubisco condensate formation by CcmM in β-carboxysome biogenesis

H. Wang, X. Yan, H. Aigner, A. Bracher, N. D. Nguyen, W. Y. Hee, B. M. Long, G. D. Price, F. U. Hartl and M. Hayer-Hartl ()
Additional contact information
H. Wang: Max Planck Institute of Biochemistry
X. Yan: Max Planck Institute of Biochemistry
H. Aigner: Max Planck Institute of Biochemistry
A. Bracher: Max Planck Institute of Biochemistry
N. D. Nguyen: Research School of Biology, The Australian National University
W. Y. Hee: Research School of Biology, The Australian National University
B. M. Long: Research School of Biology, The Australian National University
G. D. Price: Research School of Biology, The Australian National University
F. U. Hartl: Max Planck Institute of Biochemistry
M. Hayer-Hartl: Max Planck Institute of Biochemistry

Nature, 2019, vol. 566, issue 7742, 131-135

Abstract: Abstract Cells use compartmentalization of enzymes as a strategy to regulate metabolic pathways and increase their efficiency1. The α- and β-carboxysomes of cyanobacteria contain ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)—a complex of eight large (RbcL) and eight small (RbcS) subunits—and carbonic anhydrase2–4. As HCO3− can diffuse through the proteinaceous carboxysome shell but CO2 cannot5, carbonic anhydrase generates high concentrations of CO2 for carbon fixation by Rubisco6. The shell also prevents access to reducing agents, generating an oxidizing environment7–9. The formation of β-carboxysomes involves the aggregation of Rubisco by the protein CcmM10, which exists in two forms: full-length CcmM (M58 in Synechococcus elongatus PCC7942), which contains a carbonic anhydrase-like domain8 followed by three Rubisco small subunit-like (SSUL) modules connected by flexible linkers; and M35, which lacks the carbonic anhydrase-like domain11. It has long been speculated that the SSUL modules interact with Rubisco by replacing RbcS2–4. 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 eukaryotes12,13. 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 EPYC114. Understanding carboxysome biogenesis will be important for efforts to engineer CO2-concentrating mechanisms in plants15–19.

Date: 2019
References: Add references at CitEc
Citations: View citations in EconPapers (5)

Downloads: (external link)
https://www.nature.com/articles/s41586-019-0880-5 Abstract (text/html)
Access to the full text of the articles in this series is restricted.

Related works:
This item may be available elsewhere in EconPapers: Search for items with the same title.

Export reference: BibTeX RIS (EndNote, ProCite, RefMan) HTML/Text

Persistent link: https://EconPapers.repec.org/RePEc:nat:nature:v:566:y:2019:i:7742:d:10.1038_s41586-019-0880-5

Ordering information: This journal article can be ordered from
https://www.nature.com/

DOI: 10.1038/s41586-019-0880-5

Access Statistics for this article

Nature is currently edited by Magdalena Skipper

More articles in Nature from Nature
Bibliographic data for series maintained by Sonal Shukla () and Springer Nature Abstracting and Indexing ().