Hardening of bio-silica in sponge spicules involves an aging process after its enzymatic polycondensation: Evidence for an aquaporin-mediated water absorption

• Published in: Biochimica et biophysica acta Vol. 1810; no. 7; pp. 713 - 726
• Main Authors: Müller, Werner E.G., Wang, Xiaohong, Wiens, Matthias, Schloßmacher, Ute, Jochum, Klaus Peter, Schröder, Heinz C.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.07.2011
• Subjects: absorption; Absorption - drug effects; Amino Acid Sequence; Animals; aquaporins; Aquaporins - classification; Aquaporins - genetics; Aquaporins - metabolism; Bio-silica; Cathepsins - genetics; Cathepsins - metabolism; cell aggregates; Fluorescent Antibody Technique; Gene Expression - drug effects; gene expression regulation; genes; Hardening; in vitro studies; Magnesium Sulfate - pharmacology; Microscopy, Electron, Scanning; Molecular Sequence Data; Phase Transition - drug effects; Phylogeny; Primmorphs; Reverse Transcriptase Polymerase Chain Reaction; Sequence Homology, Amino Acid; Silicon Dioxide - chemistry; Silicon Dioxide - metabolism; Spectrometry, X-Ray Emission; Spicules; Sponges; Suberites - genetics; Suberites - metabolism; Suberites - ultrastructure; Suberites domuncula; Time Factors; Water - metabolism; AQP; Mn; Bio-silica; qRT-PCR; DAPI; Sponges; IEF; Spicules; Primmorphs; Hardening; Cu; TEOS; PEG; Zn; EDX; SEM; Suberites domuncula; HF; PCR; Fe
• ISSN: 0304-4165; 0006-3002; 1872-8006
• DOI: 10.1016/j.bbagen.2011.04.009

Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial. Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies. Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited. This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material. ► Sponges as a model system for evolution of metazoan body plans. ► Sponges as a model system for basic studies of skeleton formation in animals. ► Enzymatic polycondensation reaction for the formation of bio-silica. ► Expression of aquaporin gene for the first time shown during bio-silica formation. ► First description that bio-silica formation in animals requires a de-hydration step.