Matrix plasticity and the molecular basis of extracellular filament assembly in <i>Bacillus cereus</i>.

Abstract

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 <i>Bacillus cereus</i> 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.