Silica-associated proteins from hexactinellid sponges support an alternative evolutionary scenario for biomineralization in Porifera

Katsuhiko Shimizu (), Michika Nishi, Yuto Sakate, Haruka Kawanami, Tomohiro Bito, Jiro Arima, Laia Leria and Manuel Maldonado ()
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Katsuhiko Shimizu: Tottori University
Michika Nishi: Tottori University Graduate School
Yuto Sakate: Tottori University Graduate School
Haruka Kawanami: Tottori University
Tomohiro Bito: Tottori University
Jiro Arima: Tottori University
Laia Leria: Sponge Ecobiology and Biotechnology Group, Center for Advanced Studies of Blanes (CEAB, CSIC)
Manuel Maldonado: Sponge Ecobiology and Biotechnology Group, Center for Advanced Studies of Blanes (CEAB, CSIC)

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract Metazoans use silicon traces but rarely develop extensive silica skeletons, except for the early-diverging lineage of sponges. The mechanisms underlying metazoan silicification remain incompletely understood, despite significant biotechnological and evolutionary implications. Here, the characterization of two proteins identified from hexactinellid sponge silica, hexaxilin and perisilin, supports that the three classes of siliceous sponges (Hexactinellida, Demospongiae, and Homoscleromorpha) use independent protein machineries to build their skeletons, which become non-homologous structures. Hexaxilin forms the axial filament to intracellularly pattern the main symmetry of the skeletal parts, while perisilin appears to operate in their thickening, guiding extracellular deposition of peripheral silica, as does glassin, a previously characterized hexactinellid silicifying protein. Distant hexaxilin homologs occur in some bilaterians with siliceous parts, suggesting putative conserved silicifying activity along metazoan evolution. The findings also support that ancestral Porifera were non-skeletonized, acquiring silica skeletons only after diverging into major classes, what reconciles molecular-clock dating and the fossil record.

Date: 2024
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DOI: 10.1038/s41467-023-44226-7

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