Many prokaryotes form Bacterial Microcompartments (BMCs) that encapsulate segments of specialized metabolic pathways to enhance catalysis. The various functions of metabolosomes, catabolic BMCs, are dictated by the signature enzyme that processes initial substrates of the confined pathway. The components and native functions of several metabolosomes have been experimentally characterized; however one of the most prevalent across all bacteria has yet to be studied. Sugar Phosphate Utilizing (SPU) BMC loci encode enzymes predicted to be involved in sugar phosphate metabolism. The SPU genetic loci are found in organisms occupying habitats ranging from soils to hot springs, highlighting the ubiquity of the SPU BMC. We bioinformatically characterized seven SPU subtypes, all which contain an enzyme unique to SPU BMCs, a deoxyribose 5-phosphate aldolase (DERA). Here, we define the fundamental characteristics of SPU BMCs and have expressed, purified, and characterized a set of SPU core enzymes. These include a protein-protein complex formed between a SPU BMC DERA and a predicted ribose 5-phosphate isomerase. Further, we show that the SPU BMC DERA is catalytically active and propose that it acts as the universal signature enzyme for the SPU BMC, with implications for fundamental understanding and biotechnological applications of SPU BMCs.