The metabolic network response and tolerance mechanism of Thalassia hemprichii under high sulfide based on widely targeted metabolome and transcriptome

The costal eutrophication induced by human activities leads to increased sulfide level in sediments, which has been identified to cause great decline of global seagrass beds. The seagrass Thalassa hemprichii, one of the tropical dominant seagrasses in the Indo-Pacific, is facing a potential threat from sulfide, which could be easily reduced from sulfate in porewater induced by global climate change and eutrophication. However, its response and tolerance mechanism of metabolism to high sulfide is unclear. Thus, the current study investigated the physiological response and programmed metabolic network of T. hemprichii by mesocosm experiment for 3 weeks using combined physiology, stable isotopes, widely targeted metabolomics, transcriptomics, and microbial diversity. High sulfide reduced the sediment microbial diversity, while enhanced sediment sulfate reduced bacterial and δ³⁴S. The exposure to sulfide enhanced root δ³⁴S, while decreased leaf δ³⁴S of T. hemprichii. High sulfide was shown to inhibit photosynthesis via damaging PSII, which further reduced ATP production. In turn, a large number of up-regulated differently expressed genes in energy metabolism, especially in oxidative phosphorylation, were responded to compensate high energy requirement. High sulfide also promoted autophagy by overexpressing the genes related to phagocytosis and phagolysosome. Meanwhile, metabolomic profiling revealed that the contents of many basal metabolites such as carbohydrates and amino acids were reduced in both leaves and roots, as to provide more energy and synthesize stress-responded secondary metabolites. The genes related with nitrate reduction and transportation were up-regulated to promote N uptake for sulfide detoxification. High sulfide specially enhanced thiamine in roots, while enhanced jasmonic acid and flavonoids in leaves. The distinct difference of metabolites accumulation between roots and leaves might be related with the sulfide level and growth-defense trade-off. Collectively, our work highlights the specific mechanism for response and tolerance of T. hemprichii to high sulfide, providing new insights related to the seagrass strategies employed to resist sulfide, and seagrass restoration by the addition of exogenous substance.