Ribosome clustering and surface layer reorganization in the microsporidian host-invasion apparatus

Abstract

During host cell invasion, microsporidian spores translocate their entire cytoplasmic content through a thin, hollow superstructure known as the polar tube. To achieve this, the polar tube transitions from a compact spring-like state inside the environmental spore to a long needle-like tube capable of long-range sporoplasm delivery. The unique mechanical properties of the building blocks of the polar tube allow for an explosive transition from compact to extended state and support the rapid cargo translocation process. The molecular and structural factors enabling this ultrafast process and the structural changes during cargo delivery are unknown. Here, we employ light microscopy and in situ cryo-electron tomography to visualize multiple ultrastructural states of the polar tube, allowing us to evaluate the kinetics of its germination and characterize the underlying morphological transitions. We describe a cargo-filled state with a unique ordered arrangement of microsporidian ribosomes, which cluster along the thin tube wall, and an empty post-translocation state with a reduced diameter but a thicker wall. Together with a proteomic analysis of endogenously affinity-purified polar tubes, our work provides comprehensive data on the infection apparatus of microsporidia and demonstrates that ribosomes are efficiently transported through polar tubes in a spiral-like parallel arrangement.

Functional annotation of a divergent genome using sequence and structure-based homology

“…We also showed that PTP4-6 are members of the RBL family, which may contain additional, yet uncharacterized proteins that form part of the unique microsporidian infection apparatus. A recent study identified multiple RBL proteins as interaction partners of V. necatrix PTP3 ( 80 ), one of the main components of the polar tube ( 81 ). Our findings of the close relationship between PTP4-6 and RBL proteins, and the interaction of various RBL proteins with the microsporidian polar tube indicate an important role of RBLs in microsporidian host-invasion and incentivize further experimental research on this enriched protein family in Nosematida.…”