Asgard archaea represent the closest known relatives of eukaryotes, yet their biology remains poorly understood due to slow growth rates and culturing challenges. We have cultured a novel Asgard species, Nerearchaeum marumarumayae, from stromatolite-associated microbial mats in Shark Bay, Western Australia. To probe its cellular complexity, the complete proteome was structurally modelled, generating in silico models for over 4,500 proteins, which were systematically mined for structural and functional features. This comprehensive approach revealed striking protein innovations, including a giant titin-like adhesin (>5,000 amino acids, 54 fibronectin domains), an unusual “badge” protein with a novel fold conserved across Promethearchaeaceae, several WD40 scaffold proteins, and a heterodimeric tubulin pair resembling bacterial BtubA/B. In addition, encapsulin nanocages were predicted and directly observed, supporting a role in iron storage and oxidative stress protection. Integration of these predictions with cryo-electron tomography of N. marumarumayae cells identified candidate proteins underlying the distinctive cellular characteristics, including budded vesicle chains, extracellular fibres, and intracellular tube-like assemblies. By linking proteome-wide structural predictions to unusual cellular morphologies, this work illuminates the molecular innovations that shaped Asgard archaeal biology. In the context of microbial mats, a modern analogue of ancient ecosystems, these findings provide new clues to the evolutionary pathways that enabled syntrophy and the emergence of eukaryotic cell complexity.