Gene organization and control are described by models conceived in the 1960s. These models explain basic gene regulatory mechanisms and underpin current genome annotation. However, such models struggle to explain recent genome-scale observations. For example, accounts of RNA synthesis initiating within genes, widespread antisense transcription and noncanonical DNA binding by gene regulatory proteins are difficult to reconcile with traditional thinking. As a result, unexpected observations have often been dismissed and downstream consequences ignored. In this paper I will argue that, to fully understand the biology of bacterial chromosomes, we must embrace their hidden layers of complexity.