Dimethylsulfoniopropionate (DMSP) Increases Longevity and Mitochondrial Function in Caenorhabditis elegans: Implications for the Role of the Global Sulfur Cycle in Terrestrial Ecosystems

Abstract

Dimethylsulfoniopropionate (DMSP) is a compound synthesized by marine phytoplankton that contributes to the oceanic sulfur cycle. Interestingly, DMSP has also been found in algal species and several terrestrial plants, forming part of the global sulfur cycle. However, compared to its role in the marine environment, the impact of DMSP on terrestrial ecosystems remains relatively unexplored. In this study, DMSP was shown to promote longevity and prevent age-associated functional decline in Caenorhabditis elegans (C. elegans), a soil-dwelling organism. DMSP decreased mitochondrial content and improved mitochondrial function in C. elegans at the old stage, which was via enhancing autophagy flux. It was demonstrated that DMSP significantly increased the expression of autophagy and mitophagy genes during aging. Furthermore, DMSP protected against Parkinson’s disease (PD) induced by α-synuclein (α-syn) aggregation via autophagy. Mechanistic studies showed that DMSP directly activated nuclear translocation of the Skinhead-1 (SKN-1) transcription factor from the cytoplasm. Moreover, SKN-1 was involved in DMSP-induced autophagy and played a key role in lifespan extension and α-syn clearance in C. elegans. In conclusion, DMSP delays physiological aspects of aging in C. elegans, providing insights into the interplay between the global sulfur cycle and terrestrial organisms.