Silicon uptake via the transporters SySIT-L and SyLsi-L enhances the growth and photosynthesis of Synechococcus sp. PCC 7002.

Abstract

Synechococcus, a type of picoplankton, plays a crucial role in the carbon (C) and silicon (Si) biogeochemical cycles of the ocean. Their contribution to biological Si within the oligotrophic oceans can be comparable to that of diatoms. However, the mechanisms of Si assimilation, accumulation, and its impact on cellular metabolism in Synechococcus remain poorly understood. Here, we analyzed the physiological and transcriptomic responses of a model strain Synechococcus sp. PCC 7002 in the exponential growth phase to gradient Si enrichment conditions (0, 25, 50, 120, and 200 μmol L^-1) and performed knockouts of Si transport genes SySIT-L and SyLsi-L to assess relevant function. Results showed that the specific growth rate over 5 days of cultivation was increased by up to 37% in response to Si enrichment under the concentration of 120 μM, accompanied by the physiological parameters, such as cellular content of biological Si and chlorophyll a, as well as elevated rates of photosynthetic O₂ evolution and dark respiration, both of which increased with increasing ambient Si concentration especially on day 1. These changes were corroborated by the transcriptomic analysis. Knockout of the SySIT-L and SyLsi-L genes reduced the cellular Si content by ~80% both on days 1 and 5. Additionally, we found that two Si transporters were widespread in 469 sequenced cyanobacterial genomes. This study provides new scientific evidence from physiological and metabolic perspectives on the role of Synechococcus in the marine Si and C cycles, serving as a valuable starting point for exploring the mechanisms of Si metabolism in picoplankton.IMPORTANCEThis work first reveals the silicon uptake in Synechococcus PCC 7002 via two silicon transporters SIT-L and Lsi-L, which are widely distributed in 469 sequenced cyanobacterial genomes. This enhances photosynthesis and respiration, thus promoting cell growth. Our study serves as a valuable starting point for exploring the mechanisms of silicon metabolism in Synechococcus, providing biological evidence to explain the silicon accumulation of cyanobacteria in the oceans.