In response to environmental stresses such as starvation, many bacteria facultatively aggregate into multicellular structures that can attain new metabolic functions and behaviors. Despite the ubiquity and relevance of this form of collective behavior, we lack an understanding of how the spatiotemporal dynamics of aggregate development emerge from cellular physiology. Here, we study the development of multicellular aggregates by the marine bacterium Vibrio splendidus when it grows on the polysaccharide alginate. Transcriptional profiling was used to define genes differentially expressed at stages of aggregate morphogenesis, and between cell sub-populations, which included genes encoding a putative type IV pillus and carbon storage granules. Combined with measurements of in situ cellular physiology, we show that the coupling between growth and spatial gradient formation leads to the emergence of a complex lifecycle. Overall design: Comparison of samples taken from early and late stages of aggregate development. Late stage taken after structures rupture, and represents 'shell' and released inner 'core' contents.