Fossil Evidence Reveals Multiciliated Epidermal Cells Controlled Shell Mineral-Ization in Early Cambrian Acrotretoid Brachiopods

The construction of organic-inorganic composite exoskeletons through precise tissue control in eumetazoans represents one of the major innovations in the history of life. Among these organisms, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most remarkable shell structures is the organo-phosphatic cylindrical column. However, the secretion mechanisms and mineralization principles underlying these structures remain unclear. Here, for the first time, we report various types of epithelial cell moulds (squamous, cuboidal, and columnar) preserved in early Cambrian acrotretoid brachiopod fossils, along with finely preserved microscopic mineralized structures within the shell. Furthermore, submicron-scale canal structures were found in some of the cell moulds. Based on morphological similarities with the extant brachiopod Lingula anatina, we infer that early Cambrian acrotretoid brachiopods possessed multiciliated epithelial cells. Differences in the distribution of the different epithelial cell types identified herein may potentially be responsible for regulating the overall morphology of E. zhenbaensis, with columnar impressions concentrated on the highly conical ventral valve and squamous cells more prevalent on the generally flattened dorsal valve. This new finding suggests that the formation of the acrotretoid brachiopod shell was collectively controlled by epithelial cells and ciliary activities. Detailed examination of these cell impressions not only established that epithelial tissues were already well-developed in Cambrian animals, but also provides valuable insights into the mineralization mechanisms that produce exoskeletal shells.