Light‐controlled carotenoid transfer between water‐soluble proteins related to cyanobacterial photoprotection. (22nd March 2019)

• Record Type: Journal Article
• Authors: Slonimskiy, Yury B.; Muzzopappa, Fernando; Maksimov, Eugene G.; Wilson, Adjélé; Friedrich, Thomas; Kirilovsky, Diana; Sluchanko, Nikolai N.
• Is Part Of: FEBS journal. Volume 286:Number 10(2019)
• Page Start: 1908
• Page End: 1924
• Publication Date: 2019-03-22
• Subjects: carotenoid transfer -- oligomeric structure -- orange carotenoid protein -- photoprotection -- protein–protein interactions; Biochemistry -- Periodicals; Molecular biology -- Periodicals; Pathology, Molecular -- Periodicals; 572
• DOI: 10.1111/febs.14803
• Languages: English
• ISSNs: 1742-464X

Abstract

Abstract : Carotenoids are lipophilic pigments with multiple biological functions from coloration to vision and photoprotection. Still, the number of water‐soluble carotenoid‐binding proteins described to date is limited, and carotenoid transport and carotenoprotein maturation processes are largely underexplored. Recent studies revealed that CTDHs, which are natural homologs of the C‐terminal domain (CTD) of the orange carotenoid protein (OCP), a photoswitch involved in cyanobacterial photoprotection, are able to bind carotenoids, with absorption shifted far into the red region of the spectrum. Despite the recent discovery of their participation in carotenoid transfer processes, the functional roles of the diverse family of CTDHs are not well understood. Here, we characterized CTDH carotenoproteins from Anabaena variabilis (AnaCTDH) and Thermosynechococcus elongatus and examined their ability to participate in carotenoid transfer processes with a set of OCP‐derived proteins. This revealed that carotenoid transfer occurs in several directions guided by different affinities for carotenoid and specific protein–protein interactions. We show that CTDHs have higher carotenoid affinity compared to the CTD of OCP from Synechocystis, which results in carotenoid translocation from the CTD into CTDH via a metastable heterodimer intermediate. Activation of OCP by light, or mutagenesis compromising the OCP structure, provides AnaCTDH with an opportunity to extract carotenoid from the full‐length OCP, either from Synechocystis or Anabaena . These previously unknown reactions between water‐soluble carotenoproteins demonstrate multidirectionality of carotenoid transfer, allowing for efficient and reversible control over the carotenoid‐mediated protein oligomerization by light, which gives insights into the physiological regulation of OCP activity by CTDH and suggests multiple applications. Abstract : Light absorption triggers opening of the two‐domain orange carotenoid protein (OCP) and reversible translocation of the embedded carotenoid into the N‐terminal domain (NTD). Natural homologs of OCP's C‐terminal domain (CTDH) were shown to donate carotenoids to OCP or NTD homologs. Here, we demonstrate multidirectional carotenoid transfer processes between OCP‐related proteins including light‐controlled transfer from OCP to the CTD homologs (CTDHs).