Microorganisms are capable of remarkable social behaviours, such as forming transient multicellular assemblages with properties and adaptive abilities exceeding those of individual cells. Here, we report on the formation and structure of genets known as symplasmata produced by Pantoea eucalypti bacteria. Each symplasmatum develops clonally and stochastically from a single bacterium into a membrane-delimited, capsule-embedded cluster of progeny cells and with a frequency that depends on temperature, pH, and nutrient availability. Transposon mutagenesis identified several gene products required for symplasmata formation, including master regulator LrhA, replication inhibitor CspD, polysaccharide transporter RfbX3, and autoinducer synthase PhzI. We also show that bacteria inside symplasmata are shaped irregularly with punctuated cell-to-cell contacts, metabolically responsive to environmental stimuli, dispersal-ready, and transcriptionally reprogrammed to anticipate multiple alternative futures in terms of carbon source availability. The structured and conditionable nature of symplasmata offers exciting prospects towards a mechanistic understanding of multicellular behaviours and their ecological significance.