A model for the effects of germanium on silica biomineralization in choanoflagellates

Abstract

Silica biomineralization is a widespread phenomenon of major biotechnological interest. Modifying biosilica with substances like germanium (Ge) can confer useful new properties, although exposure to high levels of Ge disrupts normal biosilicification. No clear mechanism explains why this disruption occurs. Here, we study the effect of Ge on loricate choanoflagellates, a group of protists that construct a species-specific extracellular lorica from multiple siliceous costal strips. High Ge exposures were toxic, whereas lower Ge exposures produced cells with incomplete or absent loricae. These effects can be ameliorated by restoring the germanium : silicon ratio, as observed in other biosilicifying organisms. We developed simulations of how Ge interacts with polymerizing silica. In our models, Ge is readily incorporated at the ends of silica forming from silicic acid condensation, but this prevents further silica polymerization. Our ‘Ge-capping’ model is supported by observations from loricate choanoflagellates. Ge exposure terminates costal strip synthesis and lorica formation, resulting in disruption to cytokinesis and fatal build-up of silicic acid. Applying the Ge-capping model to other siliceous organisms explains the general toxicity of Ge and identifies potential protective responses in metalloid uptake and sensing. This can improve the design of new silica biomaterials, and further our understanding of silicon metabolism.

The requirement for calcification differs between ecologically important coccolithophore species

“…We presume that coccolithophores have a low requirement for Si, and it takes many generations for the intracellular pool of Si to become fully depleted. The rapid impact of Ge treatment (compared with Si limitation) suggests that Ge does not simply act as a competitive inhibitor of Si uptake, but also acts to disrupt the intracellular role of Si, as observed in diatoms and choanoflagellates (Azam & Volcani, ; Marron et al ., ).…”

Intraspecific interactions between algae with different nutritional histories

“…The lack of coupling between silicification and growth for the little silicified species Phaeodactylum tricornutum has been previously reported (De Martino et al 2007). At this stage, also in the view of the unresolved physiological effect of Ge oxides (but see Marron et al 2016), it is hard to propose an explanation for the prevalence of GeO 2grown cells over 1 mM NH 4 + -grown cells. However, Ge was found to exert an antioxidant activity on terrestrial plants (Liu et al 2016).…”

“…At this stage, also in the view of the unresolved physiological effect of Ge oxides (but see Marron et al. ), it is hard to propose an explanation for the prevalence of GeO 2 ‐grown cells over 1 mM NH 4 + ‐grown cells. However, Ge was found to exert an antioxidant activity on terrestrial plants (Liu et al.…”

Different Nutritional Histories Affect the Susceptibility of Algae to Grazing

“…This treatment was aimed at obtaining cells with a lower amount of silica, since GeO 2 is reported to impede biosilicification (Lewin ), possibly by blocking silica polymerization (Marron et al. ). 0.5 mM NH 4 + treatment (L‐NH 4 + ): the culture medium contained NH 4 + instead of NO 3 − , but the same N concentration of control conditions. 1 mM NH 4 + treatment (H‐NH 4 + ): the culture medium differed from control conditions in both the N source (NH 4 + rather than of NO 3 − ) and the N concentration (1 mM instead of 0.5 mM).…”