The Evolution of Silicon Transport in Eukaryotes

Abstract

Biosilicification (the formation of biological structures from silica) occurs in diverse eukaryotic lineages, plays a major role in global biogeochemical cycles, and has significant biotechnological applications. Silicon (Si) uptake is crucial for biosilicification, yet the evolutionary history of the transporters involved remains poorly known. Recent evidence suggests that the SIT family of Si transporters, initially identified in diatoms, may be widely distributed, with an extended family of related transporters (SIT-Ls) present in some nonsilicified organisms. Here, we identify SITs and SIT-Ls in a range of eukaryotes, including major silicified lineages (radiolarians and chrysophytes) and also bacterial SIT-Ls. Our evidence suggests that the symmetrical 10-transmembrane-domain SIT structure has independently evolved multiple times via duplication and fusion of 5-transmembrane-domain SIT-Ls. We also identify a second gene family, similar to the active Si transporter Lsi2, that is broadly distributed amongst siliceous and nonsiliceous eukaryotes. Our analyses resolve a distinct group of Lsi2-like genes, including plant and diatom Si-responsive genes, and sequences unique to siliceous sponges and choanoflagellates. The SIT/SIT-L and Lsi2 transporter families likely contribute to biosilicification in diverse lineages, indicating an ancient role for Si transport in eukaryotes. We propose that these Si transporters may have arisen initially to prevent Si toxicity in the high Si Precambrian oceans, with subsequent biologically induced reductions in Si concentrations of Phanerozoic seas leading to widespread losses of SIT, SIT-L, and Lsi2-like genes in diverse lineages. Thus, the origin and diversification of two independent Si transporter families both drove and were driven by ancient ocean Si levels.

Biosilicification Drives a Decline of Dissolved Si in the Oceans through Geologic Time

“…This challenges the hypothesis that the Precambrian oceans were controlled only by inorganic reactions. Instead, we suggest that oceanic DSi concentrations have both influenced and been influenced by the appearance and diversification of the Silicon Transporter (SIT) gene family roughly 2 billion years before the Phanerozoic (Marron et al, 2016).…”

“…Today this cyanobacterial group accounts for 25% of oceanic net primary production (Flombaum et al, 2013). Marron et al (2016) has observed SIT-like (SIT-L) genes in two strains of Synechococcus. These Si transporters probably arose initially to prevent intracellular Si toxicity in the high DSi Precambrian oceans (Marron et al, 2016), meaning that they were used to transport Si out of the cell, or to sites where Si could be safely accumulated and sequestered.…”

“…These Si transporters probably arose initially to prevent intracellular Si toxicity in the high DSi Precambrian oceans (Marron et al, 2016), meaning that they were used to transport Si out of the cell, or to sites where Si could be safely accumulated and sequestered. This would have been critical for survival, for in the absence of such a Si homeostasis mechanisms DSi could diffuse into cells from the surrounding DSi saturated seawater and reach concentrations where it would precipitate freely within the cytoplasm, interfering with cellular processes and disabling the functioning of the cell (Marron et al, 2016). Si transporting proteins can also have the ability to move other metalloids such as Ge (Durak et al, 2016) and As (Ma et al, 2008) across the cell membrane.…”

“…In our analysis here, based on advances from fields ranging from biogeochemistry (Baines et al, 2012;Frings et al, 2016) to geogenomics (Baker et al, 2014;Marron et al, 2016), we assess our state of knowledge of the global Si cycle emphasizing the substantial advances that have emerged in the past quarter of a century. We will explore the possible levels of DSi in the oceans over geologic time based on evidence from the geologic record as well as concerning the evolution of the SIT gene family.…”

Assessing the Potential of Sponges (Porifera) as Indicators of Ocean Dissolved Si Concentrations

“…Maldonado et al (1999) also showed that secretion of certain spicule types is regulated by dSi thresholds and suggested that instances of these spicules in fossil sponges reflect dSi replete environments. Efficient mechanisms to utilize dSi have evolved in sponges (Müller et al, 2003;Schröder et al, 2004;Wang et al, 2012a,b) and involve the presence of silicatein, an enzyme that is able to control and catalyze the intracellular deposition of dSi from an unsaturated environment, as well as proteins that actively transport dSi across the cell membranes (Schröder et al, 2004;Marron et al, 2016).…”