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

Hongyuan Li; Peng Ji; Yue Cao; Zhitao Cui; Jingwei Gao; Hongshuang Wang; Cong Lin; Yibo Wang; Xiaohui Wang

doi:10.1021/envhealth.3c00208

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

Environ Health (Wash). 2024 May 17;2(8):572-585. doi: 10.1021/envhealth.3c00208. eCollection 2024 Aug 16.

Authors

Hongyuan Li¹, Peng Ji², Yue Cao¹, Zhitao Cui³, Jingwei Gao^{1

4}, Hongshuang Wang¹, Cong Lin¹, Yibo Wang¹, Xiaohui Wang^{1

4

5}

Affiliations

¹ Laboratory of Chemical Biology, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, China.
² The Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University, Changchun 130024, China.
³ Department of Geriatrics, The First Hospital of Jilin University, Changchun 130021, China.
⁴ School of Applied Chemistry and Engineering, University of Science and Technology of China, Hefei 230026, China.
⁵ Beijing National Laboratory for Molecular Sciences, Beijing 100190, China.

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.