The efficient and green remediation of petroleum hydrocarbon (PH) contamination has emerged as a viable strategy for environmental management. Here, we investigated the interaction between arsenic and PH degradation by Rhodococcus sp. 2021 under their combined pollution. The strain exhibited disparate responses to varying concentrations and valences of arsenic. The elevated concentration of arsenic (>100 mg/L) facilitated the degradation of PHs, and there was a positive correlation between arsenic-promoted degradation of PHs and their carbon-chain length. The degradation of PHs changed with arsenic conditions as follows: trivalent arsenic groups > pentavalent arsenic groups > arsenic-free groups (control). Arsenite and arsenate significantly promoted the gene expression of arsenic metabolism and alkane degrading. But unlike arsenite, arsenate also significantly promoted the gene expression of phosphate metabolism. And arsenite promoted the up-regulation of the expression of genes involved in the process of PHs oxidation and fatty acid oxidation. These results highlight the potential of Rhodococcus sp. 2021 in the remediation of combined total petroleum hydrocarbon (TPH) and heavy metal pollution, providing new insights into the green and sustainable bioremediation of combined pollution of organic matters such as PHs and heavy metals/heavy metal-like elements such as arsenic.

Polycyclic aromatic hydrocarbons (PAHs)-contaminated soils are often concomitantly polluted with heavy metals, which form combined contamination through cation–π interactions and other mechanisms. However, the mechanism by which bacteria degrade PAHs under combined pollution conditions remains insufficiently studied. In this study, a benzo[a]pyrene (BaP)-degrading bacterial strain, Rhodococcus sp. PDS1, was isolated from the co-contaminated soil of an abandoned coking plant in a steel factory. This strain can not only detoxify arsenic via reductive transformation, but also mediate extracellular arsenic oxidation and efficiently degrade BaP, a high-molecular-weight (HMW) polycyclic aromatic hydrocarbon with low bioavailability and high toxicity. Response surface methodology (RSM) experiments were conducted to optimize the degrading conditions of strain PDS1, considering four factors: pH, temperature, BaP concentration, and trivalent arsenic As(III) concentration. The results showed that the BaP removal by PDS1 would reach 93.59% under the RSM-obtained optimal conditions: pH 7.7, BaP concentration 8.96 mg/L, As(III) concentration 0.82 mM, and culture temperature 36.0 °C. The transcriptome of the strain under the combined stress of arsenic and BaP was further analyzed. The results indicated that the introduction of arsenic induced the upregulated expression of different genes in the arsenic detoxification ars operon and the pcaH/G gene (encoding protocatechuate 3,4-dioxygenase, a key enzyme in BaP degradation) to varying degrees. These findings clarify the mechanism of the degradation of HMW-PAHs such as BaP by strain PDS1 under PAHs–arsenic combined pollution, lay a solid theoretical foundation for subsequent practical applications, and demonstrate the broad prospects of strain PDS1 in the remediation of actual complex contaminated soils.