Bacteria play an integral role in shaping plant growth and development. However, the genetic factors that facilitate plant-bacteria interactions remain largely unknown. Here, we demonstrated the importance of two bacterial genetic factors that facilitate the interactions between plant-growth-promoting (PGP) bacteria in the genus Caulobacter and the host plant Arabidopsis. Using homologous recombination, we disrupted the cytochrome ubiquinol oxidase (cyo) operon in both C. vibrioides CB13 and C. segnis TK0059 by knocking out the expression of cyoB (critical subunit of the cyo operon) and showed that the mutant strains were unable to enhance the growth of Arabidopsis. In addition, disruption of the cyo operon, metabolomic reconstructions, and pH measurements suggested that both elevated cyoB expression and acid production by strain CB13 contribute to the previously observed inhibition of Arabidopsis seed germination. We also showed that the crescent shape of the PGP bacterial strain C. crescentus CB15 contributes to its ability to enhance plant growth. Thus, we have identified specific genetic factors that explain how select Caulobacter strains interact with Arabidopsis plants.