Pseudosulfitobacter pseudonitzschiae hitchhikes on gliding colonies of Cellulophaga lytica

Interspecies interactions shape microbial communities; this is central for microbial ecology. Cellulophaga lytica PlyA2 is a marine flavobacterium, which glides over surfaces and forms ordered, structurally coloured colonies, which display angle-dependent reflection of light. Pseudosulfitobacter pseudonitzschiae SW is an apparently nonmotile, nonstructurally coloured marine bacterium. Here, we aim to understand the interaction of both strains at cellular, genomic, optical, and proteomic levels. Cocultivation on agar showed that P. pseudonitzschiae uses gliding C. lytica to spread by microbial hitchhiking in which Pseudosulfitobacter appears to "surf" on basal layers of motile Cellulophaga. This dispersal mechanism was found to be often beneficial for P. pseudonitzschiae, which could maximally expand its population up to 350-fold relative to monoculture. Coculture was often of limited benefit for C. lytica, only in extended cultivation on rich medium was the presence of P. pseudonitzschiae detrimental to its viability. The proteome of P. pseudonitzschiae was strongly impacted by the association with C. lytica. Quorum-sensing signalling, potential exchange of amino acids, vitamins, and other metabolites are likely mediating this hitchhiking interaction. In contrast, C. lytica made minimal adjustments to its proteome composition in coculture. Supported by optical analysis, P. pseudonitzschiae patterned C. lytica by changing how groups of the latter organised to reflect light. Our results underscore the unusual, dynamic interplay between two bacterial species and provide insights on the mechanisms underlying this relationship.