The evaluation of biogenic silica in brackish and freshwater strains reveals links between phylogeny and silica accumulation in picocyanobacteria

Abstract

Through biosilicification, organisms incorporate dissolved silica (dSi) and deposit it as biogenic silica (bSi), driving the silicon (Si) cycle in aquatic systems. While Si accumulation in marine picocyanobacteria has been recently observed, its mechanisms and ecological implications remain unclear. This study investigates biosilicification in marine and brackish picocyanobacteria of the Synechococcus clade and two model freshwater coccoid cyanobacteria. Brackish strains showed significantly higher Si quotas when supplemented with external dSi (100 µM) compared to controls (up to 60.0 ± 7.3 amol Si.cell-1 versus 9.2 to 16.3 ± 2.9 amol Si.cell-1). Conversely, freshwater strains displayed no significant differences in Si quotas between dSi-enriched treatments and controls, emphasizing that not all phytoplanktons without an obligate Si requirement accumulate this element. The Si-accumulating marine and brackish picocyanobacteria clustered within the Synechococcus clade, whereas their freshwater counterparts formed a distinct sister group, suggesting a link between phylogeny and silicification. Rapid culture growth caused increased pH and led to dSi precipitation, influencing apparent dSi uptake; this was mitigated by pH control through bubbling. This phenomenon has significant implications for natural systems affected by phytoplankton blooms. In such environments, pH-induced silicon precipitation may reduce dSi availability impacting Si-dependent populations like diatoms. Our findings suggest brackish picocyanobacteria could significantly influence the Si cycle through at least two mechanisms: cellular Si accumulation and biologically induced changes in dSi concentrations.IMPORTANCEThis work provides the first evidence of biogenic silica accumulation in brackish picocyanobacteria and uncovers a link between phylogeny and biosilicification patterns. Our findings demonstrate that picocyanobacterial growth induces pH-dependent silica precipitation, which could lead to overestimations of cellular Si quotas by up to 85%. This process may drive substantial silica precipitation in highly productive freshwater and coastal marine systems, with potential effects on silica cycling and the population dynamics of Si-dependent phytoplankton. The extent of biosilicification in modern picocyanobacteria offers insights into the rock record, shedding light on the evolutionary and ecological dynamics that influence sedimentary processes and the preservation of biosilicification signatures in geological formations. Overall, this research adds to the significant impact that microorganisms lacking an obligate silica requirement may have on silica dynamics.

Keywords: Synechococcus; biosilicification; brackish picocyanobacteria; silicon accumulation.

Fig 1

Growth curves, pH, and cellular silicon content in batch cultures of a marine (WH 5701) and three brackish (BA 120, BA 124, and BA 132) picocyanobacteria. (a) Growth curves of picocyanobacteria cultured in dSi-enriched media (+100 µM); (b) pH evolution in cultures of picocyanobacteria cultured in dSi-enriched media; (c) cellular silicon accumulation in control conditions (without added dSi) and in dSi-enriched media. The arrows indicate the time point at which the samples were collected for bSi analysis.

Fig 2

Growth and cellular silicon content in picocyanobacterial strains in bubbled or cultures buffered with HEPES. Growth curves of brackish strains BA 120 (a), BA 124 (b), and marine strain WH 5701 (c); (d) cellular silicon accumulation in strains cultured in dSi-enriched media (+100 µM) in bubble cultures or buffered with HEPES pH 7.5 5 mM or 10 mM. ns, not significant; letters a and b denote statistical differences (one-way ANOVA, P < 0.05; Tukey post-hoc P < 0.05). The arrows indicate the time point at which samples were collected for bSi analysis.

Fig 3

Cellular silicon content in marine, brackish, and freshwater strains. Strains were cultured in control conditions (without added dSi) and in dSi-enriched media (+100 μM). Asterisk(s) (*) indicate significant P values (one-way ANOVA, *P ≤ 0.05, **P ≤ 0.01, and ***P ≤ 0.001).

Fig 4

Phylogenetic position of picocyanobacterial strains used in this study and other strains shown to accumulate Si. Red circles indicate strains harboring SIT-Ls (17), and strains in blue were previously shown to accumulate Si (5). Stars indicate strains tested for Si accumulation in this study: yellow stars indicate strains that accumulated Si, and black stars indicate those that did not accumulate Si. All BA strains and KAC strains (in bold) were screened for SIT-Ls. Maximum likelihood phylogenies were constructed using a GTR + F + I + I + R3 model determined by ModelFinder (60). Bootstrap values were calculated with 1,000 replicates (58).