Sulfur-oxidizing bacteria from the SUP05 clade are abundant in anoxic and oxygenated marine waters that appear to lack reduced sources of sulfur for cell growth. This raises questions about how these chemosynthetic bacteria survive across oxygen and sulfur gradients and how their mode of survival impacts the environment. Here we use growth experiments, proteomics and cryo-electron tomography to show that a SUP05 isolate, Ca. Thioglobus autotrophicus, is several times larger, amorphous in shape and stores considerably more intracellular sulfur when it respires oxygen. We also show that these cells can use diverse sources of reduced organic and inorganic sulfur at submicromolar concentrations. Enhanced cell size, carbon content and metabolic activity of the aerobic phenotype are likely facilitated by a stabilizing surface-layer (S-layer) and an uncharacterized form of FtsZ-less cell division that supports morphological plasticity. The additional sulfur storage provides an energy source that allows cells to continue metabolic activity when exogenous sulfur sources are not available. This metabolic flexibility leads to the production of more organic carbon in the ocean than estimates that are based solely on their anaerobic phenotype.