Synechococcus transcriptomes to examine the mechanism of silicification in picocyanobacteria. Syn-Si

Through biosilicification, organisms incorporate dissolved silica (dSi) and deposit it in the form of biogenic silica (bSi). By assimilating dSi, eukaryotes drive the silicon (Si) cycle in aquatic systems. While Si accumulation has been recently observed in highly abundant marine picocyanobacteria, the mechanisms and ecological implications remain poorly constrained. In this study, we explored the mechanisms underlying biosilicification in marine and brackish picocyanobacteria strains belonging to the Synechococcus clade and model freshwater coccoid cyanobacteria. Also, we combined molecular, biochemical, and bioinformatic approaches to examine the mechanism of silicification in picocyanobacteria, currently not fully understood. Cellular Si quotas in the brackish strains were significantly higher in cultures supplemented with external dSi (100 µM) compared to controls (up to 60.02 ± 7.32 amol Si.cell-1 versus 9.20 to 16.3 ± 2.9 amol Si.cell-1 in the controls). In contrast, the freshwater strains showed no differences in Si quotas between dSi-enriched treatments and controls. Whole transcriptomic analysis revealed no differences in gene expression between Si-treated and non-treated cell cultures, which suggests that Si addition does not affect cell metabolism. Marine and brackish picocyanobacteria accumulating Si fell within the Synechococcus clade whereas freshwater counterparts formed a sister group, which suggests a potential link between phylogeny and silicification in terms of strain response to external dSi concentration. Rapidly growing cultures led to pH increases and subsequent dSi precipitation, influencing the apparent dSi uptake, which was avoided when pH was controlled by bubbling the cultures. Our findings point toward a scenario in which brackish picocyanobacteria could play a significant role in the Si cycle through at least two mechanisms: cellular Si accumulation and biologically-induced dSi precipitation.