Facultative phototrophic bacterium Rhodobacter capsulatus DsbA-null mutants are proficient in photosynthesis but are defective in respiration, especially in enriched growth medium at 35 ºC. They also exhibit severe pleiotropic phenotypes extending from motility defects to osmo-fragility and oxidative stresses. In this work, using a combined proteomic and molecular genetic approach, we demonstrate that the respiratory defect of R. capsulatus DsbA-null mutants originates from the overproduction of the periplasmic protease DegP, which renders them temperature sensitive for growth. The DsbA-null mutants revert frequently to overcome this growth defect by decreasing, but not completely eliminating, their DegP activity. In agreement with these findings, we show that overproduction of DegP abolishes the newly restored respiratory growth ability of the revertants in all growth media. Structural localizations of the reversion mutations in DegP reveal the regions and amino acids that are important for its protease-chaperone activity. Remarkably, although R. capsulatus DsbA-null or DegP-null mutants are viable, DegP-null DsbA-null double mutants are lethal at all growth temperatures. This is unlike E. coli, and it indicates that in the absence of DsbA some DegP activity is required for survival of R. capsulatus. Absence of a DegQ protease homologue in some bacteria together with major structural variations amongst the DegP homologues, including a critical disulfide bond-bearing region, correlate well with the differences seen between various species like R. capsulatus and E. coli. Our findings illustrate the occurrence of two related but distinct periplasmic protease families in bacterial species.