Bacterial microcompartments (BMCs) are polyhedral, protein-based organelles present in a wide range of bacteria. This mode of compartmentalization is highly modular and can accommodate a wide range of chemistries within them, including carbon fixation. These aspects make them a promising target to serve as bioplatforms for commodity chemical synthesis and enhanced carbon fixation. However, it is challenging to investigate the structure and function of BMCs using classical methods. As such, the native structure of BMCs remains largely enigmatic, hampering their synthetic adaption. This dissertation addresses these concerns by describing the assembly state of the model 1,2-propanediol (Pdu) BMC using a variety of approaches. Chemical probing reveals the Pdu BMC is surprisingly permeable to and permissive of derivatization. This insight enabled application of crosslinking mass spectrometry to describe its protein interactome. The interactome map reveals that small domains called encapsulation peptides dominate interior interactions while reporting on the organization of the outer protein shell. Laser scanning confocal approaches were developed to study the solution behavior of BMCs. These experiments heavily suggest that the Pdu BMC is a dynamic entity that exchanges protein elements; a result we primarily attribute to the protein shell. These confocal microscopy approaches were further used to study the super-structures formed by individual shell proteins and to describe their interactions with one another. Together, the results from this project give important insight on the assembly state of the model Pdu BMC including its biogenesis, organization, and behavior. These data answer some of the open questions concerning the assembly of BMC structures, which will help innovate the next generation of BMC-based biotechnology tools.