sll1019 and slr1259 encoding glyoxalase II improve tolerance of Synechocystis sp. PCC 6803 to methylglyoxal- and ethanol- induced oxidative stress by glyoxalase pathway.

Abstract

The glyoxalase pathway is the primary detoxification mechanism for methylglyoxal (MG), a ubiquitous toxic metabolite that disrupts redox homeostasis. In the glyoxalase pathway, glyoxalase II (GlyII) can completely detoxify MG. Increasing the activity of the glyoxalase system can enhance the resistance of plants or organisms to abiotic stress, but the relevant mechanism remains largely unknown. In this study, we investigated the physiological functions of GlyII genes (sll1019 and slr1259) in Synechocystis sp. PCC 6803 under MG or ethanol stress based on transcriptome and metabolome data. High-performance liquid chromatography (HPLC) results showed that proteins Sll1019 and Slr1259 had GlyII activity. Under stress conditions, sll1019 and slr1259 protected the strain against oxidative stress by enhancing the activity of the glyoxalase pathway and raising the contents of antioxidants such as glutathione and superoxide dismutase. In the photosynthetic system, sll1019 and slr1259 indirectly affected the light energy absorption by strains, synthesis of photosynthetic pigments, and activities of photosystem I and photosystem II, which was crucial for the growth of the strain under stress conditions. In addition, sll1019 and slr1259 enhanced the tolerance of strain to oxidative stress by indirectly regulating metabolic networks, including ensuring energy acquisition, NADH and NADPH production, and phosphate and nitrate transport. This study reveals the mechanism by which sll1019 and slr1259 improve oxidative stress tolerance of strains by glyoxalase pathway. Our findings provide theoretical basis for breeding, seedling, and field production of abiotic stress tolerance-enhanced variety.IMPORTANCEThe glyoxalase system is present in most organisms, and it is the primary pathway for eliminating the toxic metabolite methylglyoxal. Increasing the activity of the glyoxalase system can enhance plant resistance to environmental stress, but the relevant mechanism is poorly understood. This study revealed the physiological functions of glyoxalase II genes sll1019 and slr1259 in Synechocystis sp. PCC 6803 under abiotic stress conditions and their regulatory effects on oxidative stress tolerance of strains. Under stress conditions, sll1019 and slr1259 enhanced the activity of the glyoxalase pathway and the antioxidant system, maintained photosynthesis, ensured energy acquisition, NADH and NADPH production, and phosphate and nitrate transport, thereby protecting the strain against oxidative stress. This study lays a foundation for further deciphering the mechanism by which the glyoxalase system enhances the tolerance of cells to abiotic stress, providing important information for breeding, seedling, and selection of plants with strong stress resistance.