Researchers from the University of Tottori (Japan) and the Center for Advanced Studies in Blanes (CEAB-CSIC) have made an unprecedented discovery shedding light on the transition from unicellular to multicellular organisms 600 million years ago.
Sponges are likely the first animals to have appeared on Earth, making them particularly interesting for clues about how multicellular animals could have evolved from an ancestral unicellular organism in the Precambrian oceans. They are also unique animals because they use dissolved silicon in water in the form of silicic acid to create architecturally impressive skeletons. These skeletons are “crystal-like,” with the same chemical composition as the glass in our windows, consisting of a compound technically known as “silica” (SiO2).
Since silica is now one of the most important industrial inorganic materials, mastering the biological process by which sponges produce it raises significant biotechnological expectations related to the development of optical fiber, materials and architectural structures, thermally stable encapsulation of viral vaccines and mRNA, and experimental bone regeneration therapies in mammals, among other possibilities. However, advances in potential applications are hampered by difficulties in spatially controlling silica deposition during the polymerization process.
Therefore, a deeper understanding of these marine animals can, on one hand, reveal evolutionary keys and, on the other, open innovative perspectives for biotechnology: knowing exactly how sponges biologically produce silica could unveil new paths for controlled synthesis of this mineral with lower cost and environmental impact than current industrial processes, representing an old biotechnological aspiration.
A study published now in Nature Communications represents a revolutionary advance in both areas. A Japanese team from the University of Tottori and a group of Spanish scientists from the CSIC, specifically from the Center for Advanced Studies in Blanes (CEAB-CSIC), have discovered two new proteins, named hexaxilin and perisilin, inside the silica of sponges. Although their biotechnological applicability will be revealed in future studies, their mere discovery is a significant breakthrough. It carries a fascinating and revolutionary message about the function of proteins and the evolution of sponge skeletons.
There are three classes of silica-producing sponges, which were assumed to use similar cellular and molecular tools for the common purpose of building a siliceous skeleton. The study now published reveals that each of the three classes of sponges has independently developed its own protein machinery to produce silica.
Manuel Maldonado, a researcher at CEAB-CSIC and the leader of the study, explains that “an important first implication of the discovery is that the siliceous skeletons of the three classes of sponges are not homologous but analogous structures developed to perform similar functions. A second important implication is that independent acquisition of silica-producing machinery can only be explained if the ancestral sponge lineage first diverged at the molecular and cellular levels to give rise to different classes, and then each class independently acquired the ability to produce siliceous skeletons. This would mean that, although most modern sponges are characterized by impressive mineral skeletons, the ancestral sponge lineage and the early members of the three siliceous classes lacked mineral skeletons.”
The confirmation of the absence of siliceous skeletons in these early sponges is a notable finding because it resolves the current conflict between molecular clocks, which estimate the origin of sponges in the Precambrian (about 850 to 650 million years ago), and fossilized mineral skeletons, which only attest to the existence of the group in the Cambrian (about 535 million years ago). The results of this study now suggest that such a conflict does not exist, and both estimates could be correct: sponges appeared and began to diversify in the Precambrian, but evolving lineages were not able to produce siliceous skeletons until the Cambrian. These discoveries enhance our understanding of the original characteristics of the earliest animal groups and how the evolutionary transition from unicellular to multicellular animal stages may have occurred.
The study also reveals that the biological production of siliceous skeletal pieces is a fairly complex process, requiring at least one protein to control silica deposition in the internal region of the structure and other proteins to subsequently add concentric layers of peripheral silica for thickening and final ornamentation of the skeletal piece. The authors note that they have detected several additional proteins in the silica of the sponges studied but could not characterize them. Therefore, future studies will be necessary not only for their characterization but also to understand how all these proteins interact in intracellular and extracellular environments during silica deposition. Overall, the findings and the new questions raised by this study open promising alternative scenarios for future research on controlled biosilica production.
Article reference: Shimizu, K., Nishi, M., Sakate, Y. et al. Silica-associated proteins from hexactinellid sponges support an alternative evolutionary scenario for biomineralization in Porifera. Nat Commun 15, 181 (2024). https://doi.org/10.1038/s41467-023-44226-7