This study investigates the transcriptional profile of a novel oil-degrading microbial consortium (MC1) composed of four bacterial isolates from Brazilian oil reservoirs: Acinetobacter baumannii subsp. oleum ficedula, Bacillus velezensis, Enterobacter asburiae, and Klebsiella pneumoniae. Genomic analysis revealed an enrichment of genes associated with xenobiotic degradation, particularly for aminobenzoate, atrazine, and aromatic compounds, compared to reference genomes. The consortium demonstrated superior growth and complete oil degradation relative to individual strains. Transcriptional profiling during growth on oil indicated that key subsystems involved membrane transport, stress response, and dehydrogenase complexes, crucial for hydrocarbon uptake. Notably, genes for degrading aromatics, naphthalene, and chloroalkanes were significantly expressed during the initial oil growth phase. The dominant gene expressed was alkane 1-monooxygenase, particularly in the late growth phase. While A. baumannii exhibited the highest transcriptional activity, B. velezensis showed lower activity despite possessing numerous hydrocarbon degradation genes. The synergistic interactions among strains, confirmed by complementary gene expression patterns, position MC1 as a promising bioremediation agent for hydrocarbon-contaminated environments. However, more than collaboration, competition for nutrient uptake and resistance to stress drive gene expression and adaptation in the presence of oil as the carbon source.