Matrix plasticity and the molecular basis of extracellular filament assembly in Bacillus cereus
- Ana Álvarez-Mena
- Muhammed Bilal Abdul Shukkoor
- Joaquín Caro-Astorga
- Mélanie Berbon
- María Luisa Antequera-Gómez
- Montserrat Grifé-Ruiz
- Axelle Grélard
- Brice Kauffmann
- Estelle Morvan
- Oscar P. Kuipers
- Antonio de Vicente
- Birgit Habenstein
- Antoine Loquet
- Diego Romero
2026-04-15
The controlled assembly of extracellular filaments is essential for bacterial multicellularity and surface colonization. While Gram-positive bacteria rely on a variety of mechanisms to construct surface-associated fibers, many noncanonical pathways remain largely unexplored. Here, we identify a regulated, sortase-independent system in Bacillus cereus that governs the polymerization of filaments within the extracellular matrix (ECM). This tripartite system comprises CapP, a chaperone-like protein, and the structural subunits TasA and CalY. CapP modulates filament formation in a concentration- and domain-dependent manner, promoting ordered heteropolymer assembly while preventing uncontrolled aggregation. Disrupting this pathway leads to distinct compensatory changes in matrix composition—including exopolysaccharide expression, extracellular DNA release, and flagellar regulation—revealing an unexpected level of matrix plasticity. Our findings uncover a unique mechanism of ECM biogenesis in Gram-positive bacteria and suggest that plasticity in matrix organization may be a widespread adaptive strategy across bacterial lineages.