Sponge fossils from the Cambrian black shales have attracted attention from both palaeontologists and geochemists for many years in terms of their high diversity, beautiful preservation and perplexing adaptation to inhospitable living environments. However, the body shape of these sponges, which contributes to deciphering adaptive evolution, has not been scrutinized. New complete specimens of the hexactinellid sponge Sanshapentella tentoriformis sp. nov. from the Qingjiang biota (black shale of the Cambrian Stage 3 Shuijingtuo Formation, ca 518 Ma) allow recognition of a unique dendriform body characterized by a columnar trunk with multiple conical high peaks and distinctive quadripod-shaped dermal spicules that frame each high peak. The body shape of this new sponge along with other early Cambrian hexactinellids, is classified into three morpho-groups that reflect different levels of adaptivity to the environment. The cylindrical and ovoid bodies generally adapted to a large spectrum of environments; however, the dendriform body of S. tentoriformis was restricted to the relatively deep-water, oxygen-deficient environment. From a hindsight view, the unique body shape represents a consequence of adaptation that helps maintain an effective use of oxygen and a low energy cost in hypoxic conditions.

Hyoliths (hyolithids and orthothecids) were one of the most successful early biomineralizing lophotrochozoans and were a key component of the Cambrian evolutionary fauna. However, the morphology, skeletogenesis and anatomy of earliest members of this enigmatic clade, as well as its relationship with other lophotrochozoan phyla remain contentious. Here, we present a new orthothecid, Longxiantheca mira gen. et sp. nov. preserved as part of secondarily phosphatized small shelly fossil assemblage from the lower Cambrian Xinji Formation of North China. Longxiantheca mira retains some ancestral traits of the clade with an undifferentiated disc-shaped operculum, a simple conical conch with apical septa and a two-layered microstructure of aragonitic fibrous bundles. The operculum interior exhibits impressions of soft tissues, including muscle attachment scars, mantle epithelial cells and a central kidney-shaped platform interpreted as a support structure in association with its presumptive feeding apparatus. The muscular system in orthothecids appears to be similar to that in hyolithids, suggesting a consistent anatomical configuration among the total group of hyoliths. The new finding of shell secreting cells demonstrates a mantle regulating the mode of growth for the operculum. Investigations of shell microstructures support the placement of hyoliths as total group molluscs with an unsettled position within the phylum Mollusca.

The Precambrian–Cambrian interval saw the first appearance of disparate modern metazoan phyla equipped with a wide array of mineralized exo- and endo-skeletons. However, the current knowledge of this remarkable metazoan skeletonization bio-event and its environmental interactions is limited because uncertainties have persisted in determining the mineralogy, microstructure, and hierarchical complexity of these earliest animal skeletons. This study characterizes in detail a previously poorly understood fibrous microstructure—the lamello-fibrillar (LF) nacre—in early Cambrian mollusk and hyolith shells and compares it with shell microstructures in modern counterparts (coleoid cuttlebones and serpulid tubes). This comparative study highlights key differences in the LF nacre amongst different lophotrochozoan groups in terms of mineralogical compositions and architectural organization of crystals. The results demonstrate that the LF nacre is a microstructural motif confined to the Mollusca. This study demonstrates that similar fibrous microstructure in Cambrian mollusks and hyoliths actually represent a primitive type of prismatic microstructure constituted of calcitic prisms. Revision of these fibrous microstructures in Cambrian fossils demonstrates that calcitic shells are prevalent in the so-called aragonite sea of the earliest Cambrian. This has important implications for understanding the relationship between seawater chemistry and skeletal mineralogy at the time when skeletons were first acquired by early lophotrochozoan biomineralizers.

The evolutionary mechanism behind the early Cambrian animal skeletonization was a complex and multifaceted process involving environmental, ecological, and biological factors. Predation pressure, oxygenation, and seawater chemistry change have frequently been proposed as the main drivers of this biological innovation, yet the selection pressures from microorganisms have been largely overlooked. Here we present evidence that calcareous shells of the earliest mollusks from the basal Cambrian (Fortunian Age, ca. 539–529 million years ago) of Mongolia developed advanced tubule systems that evolved primarily as a defensive strategy against extensive microbial attacks within a microbe-dominated marine ecosystem. These high-density tubules, comprising approximately 35% of shell volume, enable nascent mineralized mollusks to cope with increasing microbial bioerosion caused by boring endolithic cyanobacteria, and hence represent an innovation in shell calcification. Our finding demonstrates that enhanced microboring pressures played a significant role in shaping the calcification of the earliest mineralized mollusks during the Cambrian Explosion.