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The Evolution of Silicon Transport in Eukaryotes.

Published version
Peer-reviewed

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Authors

Marron, Alan O 
Ratcliffe, Sarah 
Wheeler, Glen L 
Goldstein, Raymond E 
King, Nicole 

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.

Description

Keywords

Lsi2, SIT, convergent evolution, eukaryotes, silicon, transporter., Amino Acid Sequence, Biological Evolution, Biological Transport, Carrier Proteins, Choanoflagellata, Diatoms, Eukaryota, Evolution, Molecular, Membrane Transport Proteins, Phylogeny, Sequence Analysis, DNA, Sequence Homology, Amino Acid, Silicon

Journal Title

Mol Biol Evol

Conference Name

Journal ISSN

0737-4038
1537-1719

Volume Title

33

Publisher

Oxford University Press (OUP)
Sponsorship
European Research Council (247333)
Wellcome Trust (097855/Z/11/Z)
This work was supported by the EDEN Evo-Dev-Eco Network Research Exchange Fund, the Musgrave Pratt Fund (Department of Zoology, University of Cambridge) and the Parke-Davis Fund (University of Cambridge) to AOM; the European Research Council (Advanced Investigator Grant No. 247333) and the Wellcome Trust Senior Investigator Award to AOM and REG; the European Research Council [starting grant No. 282101 to Paul Curnow under the European Union's Seventh Framework Programme (FP7/2007-2013)] (to SR); the National Environmental Research Council (grant no. NE/J021954/1) to GLW; the Howard Hughes Medical Institute to NK; the Japan Science and Technology Agency-Centre National de la Recherche Scientifique program to FN; and a National Defense Science and Engineering Graduate fellowship from the United States Department of Defense, a National Science Foundation Central Europe Summer Research Institute Fellowship, a Chang-Lin Tien Fellowship in Environmental Sciences and Biodiversity, a postdoctoral fellowship from the Conseil Régional de Bretagne, and the French Government “Investissements d’Avenir” program OCEANOMICS (ANR-11-BTBR-0008) to DJR.