Effects of PSII Manganese-Stabilizing Protein Succinylation on Photosynthesis in the Model Cyanobacterium Synechococcus sp. PCC 7002

Abstract

Lysine succinylation is a newly identified protein post-translational modification and plays important roles in various biological pathways in both prokaryotes and eukaryotes, but its extent and function in photosynthetic organisms remain largely unknown. Here, we performed the first systematic studies of lysine succinylation in cyanobacteria, which are the only prokaryotes capable of oxygenic photosynthesis and the established model organisms for studying photosynthetic mechanisms. By using mass spectrometry analysis in combination with the enrichment of succinylated peptides from digested cell lysates, we identified 1,704 lysine succinylation sites on 691 proteins in a model cyanobacterium Synechococcus sp. PCC 7002. Bioinformatic analysis revealed that a large proportion of the succinylation sites were present on proteins in photosynthesis and metabolism. Among all identified succinylated proteins involved in photosynthesis, the PSII manganese-stabilizing protein (PsbO) was found to be succinylated on Lys99 and Lys234. Functional studies of PsbO were performed by site-directed mutagenesis, and mutants mimicking either constitutively succinylated (K99E and K234E) or non-succinylated states (K99R and K234R) were constructed. The succinylation-mimicking K234E mutant exhibited a decreased oxygen evolution rate of the PSII center and the efficiency of energy transfer during the photosynthetic reaction. Molecular dynamics simulations suggested a mechanism that may allow succinylation to influence the efficiency of photosynthesis by altering the conformation of PsbO, thereby hindering the interaction between PsbO and the PSII core. Our findings suggest that reversible succinylation may be an important regulatory mechanism during photosynthesis in Synechococcus, as well as in other photosynthetic organisms.

Large-Scale Assessment of Bioinformatics Tools for Lysine Succinylation Sites

“…Nowadays, several machine learning-based predictors have been employed to identify succinylation sites [54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70]. The SucPred [54] is the first succinylation site predictor, which was established by Zhao et al in 2015 through different encoding descriptors, including position amino acids weight composition, van der Waals volume normalized, grouped weight-based encoding, and auto-correlation functions, via SVM.…”

Systematic identification and comparative analysis of lysine succinylation between the green and white parts of chimeric leaves of Ananas comosus var. bracteatus

“…In this study, the Wh parts of chimeric leaves had higher starch content and lower soluble sugar content, which suggested the Wh parts take a low photosynthetic rate and may act as a photosynthetic product sink. Previous studies have shown that lysine succinylation is prevalent in various photosynthetic organisms [8]. In this study, six succinylated proteins involved in photosynthesis were identified only in the Gr parts of chimeric leaves, including three subunits in photosystem I (PsaC, PsaD, PsaF), two subunits in photosystem II (PsbB, PsbP) and light-harvesting complex II chlorophyll a/b binding protein 2 (Lhcb2).…”

“…PsbO is the largest extrinsic subunit of PSII, which plays critical roles in oxygen evolution reaction [36]. In cyanobacterium, PsbO succinylation can hinder correct interactions between PsbO and other PSII subunits by the conformation changes in the head domain of PsbO, leading to a negative regulation of oxygen evolution [8]. However, the Ksu sites in PsbO of Ananas comosus var.…”

“…Succinylation was first reported in histone proteins, and it therefore can function in regulating gene expression through effects on chromatin structure [6]. Lysine succinylation has been studied in diverse organisms and tissues [7,8], and succinylated proteins are abundant in mitochondrial metabolism, including the CAC, amino acid degradation and fatty acid metabolism [9].…”

A Hybrid Flux Balance Analysis and Machine Learning Pipeline Elucidates Metabolic Adaptation in Cyanobacteria

“…Furthermore, these co-factors contribute to mechanisms for survival in iron-depleted environments (Palenik et al, 2003), such as the secretion of siderophores to chelate iron. In the form of the photosystem II manganese-stabilizing polypeptide (psbO), manganese plays a critical role in photosystem II function by catalyzing the light-induced dissociation of water to molecular oxygen (Bartsevich and Pakrasi, 1995;Liu et al, 2018). Inactivation of the manganese transport system (MNABC) leads to an invariable loss of activity in photosystem II, consequently affecting the photosynthetic process as a whole (Shcolnick and Keren, 2006 Table S4: Contributions of genes to variance, Related to Figure 3.…”