Lysine Propionylation is a Widespread Post-Translational Modification Involved in Regulation of Photosynthesis and Metabolism in Cyanobacteria

Mingkun Yang,Hui Huang,Feng Ge

doi:10.3390/ijms20194792

Abstract

Lysine propionylation is a reversible and widely distributed post-translational modification that is known to play a regulatory role in both eukaryotes and prokaryotes. However, the extent and function of lysine propionylation in photosynthetic organisms remains unclear. Cyanobacteria are the most ancient group of Gram-negative bacteria capable of oxygenic photosynthesis, and are of great importance to global carbon and nitrogen cycles. Here, we carried out a systematic study of lysine propionylaiton in cyanobacteria where we used Synechocystis sp. PCC 6803 (Synechocystis) as a model. Combining high-affinity anti-propionyllysine pan antibodies with high-accuracy mass spectrometry (MS) analysis, we identified 111 unique lysine propionylation sites on 69 proteins in Synechocystis. Further bioinformatic analysis showed that a large fraction of the propionylated proteins were involved in photosynthesis and metabolism. The functional significance of lysine propionylation on the enzymatic activity of fructose-1,6-bisphosphatase (FbpI) was studied by site-directed mutagenesis and biochemical studies. Further functional studies revealed that the propionylation level of subunit II of photosystem I (PsaD) was obviously increased after high light (HL) treatment, suggesting that propionylation may be involved in high light adaption in Synechocystis. Thus, our findings provide novel insights into the range of functions regulated by propionylation and reveal that reversible propionylation is a functional modification with the potential to regulate photosynthesis and carbon metabolism in Synechocystis, as well as in other photosynthetic organisms.

Highlights

Lysine propionylation is a reversible and widely distributed post-translational modification (PTM) in which a propionyl group (CH3-CH2-CO-) is added to the -amino group of lysine residue on a protein moiety [1,2]
Our results reveal the widest variety of propionylated proteins in photosynthetic organisms presently available, and offer insights into the functions related to propionylation in cyanobacteria
Propionylation signals were abundant and likely to be changed for several protein bands in the 10–55 kDa mass range in Synechocystis under different stress conditions. These results implied that lysine propionylation is a widespread protein modification and is likely to be involved in stress responses in Synechocystis

Summary

Introduction

Lysine propionylation is a reversible and widely distributed post-translational modification (PTM) in which a propionyl group (CH3-CH2-CO-) is added to the -amino group of lysine residue on a protein moiety [1,2]. Comprehensive studies have focused on identifying the propionylated proteins in Thermus thermophilus [3], Mycobacterium tuberculosis [4], yeast [5], mammalian cells [1,6], and mouse liver mitochondria [7], as well as the enzymes that are responsible for adding and removing this modification, including p300 [1,2,6], CREB-binding protein [1,2], Sirt1 [1], Sirt2 [6,8], Sirt3 [8], Pat [8], AcuA [8], and CobB [8] These studies have demonstrated that lysine propionylation occurs in a diverse range of proteins and exerts influence on a wide range of biological functions. These findings strongly suggest that lysine propionylation is likely to be one of the mechanisms that regulates cellular metabolism and responds to stress conditions in both bacteria and mammals [3,7]

Methods

Results

Conclusion