Evidence for two independent ecological roles of dimethylsulfoniopropionate (DMSP)

Dimethylsulfoniopropionate (DMSP) is a labile sulfur and carbon metabolite that significantly contributes to both the cycling of marine dissolved organic carbon and the balance of Earth’s albedo. DMSP is produced by a diverse array of marine microbes, but despite decades of research, the cellular mechanism and environmental drivers of DMSP production remain unknown. Previous work has searched for a universal function of DMSP. We used physiological experiments, -omics surveys and a global ecosystem model to demonstrate that DMSP serves two different ecological roles. Specifically, with targeted physiological experiments that compared different cellular metabolic conditions, we show that high DMSP producers (HiDPs) (e.g. haptophytes) constitutively produce DMSP, whereas low DMSP producers (LoDPs) (e.g. diatoms) dynamically regulate DMSP as a function of environmental stress. Furthermore, we found that two recently described DMSP synthesis genes are widespread and similarly differentiated across taxonomic groups in both monocultures and in situ. This suggests that the observed DMSP phenotypes are regulated by two distinct genes that evolved separately. Finally, with natural community incubations and a global ecosystem model, we show that HiDPs dominate in situ DMSP production and therefore determine large scale patterns of in situ DMSP variability. In contrast, the fine-tuned regulation of DMSP by LoDPs is likely more important for microbial interactions as a signaling molecule at the microscale. This new paradigm of differential regulation by HiDPs and LoDPs that results in two independent ecological roles should be considered when quantifying the contribution of DMSP to global carbon cycling and climate regulation.