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Toluene and xylenes are environmental pollutants. The xyl upper operon, comprising seven genes (xylUWCMABN), plays a crucial role in converting toluene and xylenes into benzoate and its methyl derivatives. In this study, we employed a bioinformatics strategy to investigate the xyl upper operon across diverse taxonomic lineages, encompassing over 500,000 genomes representing 206 phyla and at least 4357 genera. Results revealed the presence of xyl upper operons in 58 bacterial genomes, spanning distant species from 13 genera, with an average nucleotide identity (ANI) and average amino acid identity (AAI) as low as 66.90% and 55.85%, respectively. Among the scrutinized genomes, 10 of them were complete revealing two xyl upper operons on plasmids and eight on bacterial chromosomes. Importantly, the gene organization within the xyl upper operon remained remarkably conserved. Noteworthy findings also included a high abundance of ISL3, IS5, and IS1380 family transposases near these operons, suggesting their potential role in facilitating the dissemination of the xyl upper operon among different bacterial strains. Phylogenetic analysis of the xylM gene revealed three distinct monophyletic clades, highlighting diversity within this gene. The results implied the dissemination potential of xyl upper operons in distant species, as well as transition from plasmids to chromosomes. Furthermore, we confirmed the genetic background differences between the upper and lower xyl operons in a wider range of species. This comprehensive understanding of the genetic basis of the xyl upper operon contributes valuable insights for the microbial degradation of toluene and xylene. • The xyl upper operons are responsible for degradation of toluene and xylenes. • The organization of genes in xyl upper operons are highly conserved. • The xyl upper operons are distributed on either plasmid or chromosome. • Transposases were responsible for the dissemination of xyl upper operons. • Three mono clades of the xylM gene were observed. [ABSTRACT FROM AUTHOR]

[Display omitted] • Hydrocarbon-degrading consortia were dominated by homogeneous dispersal processes; • Nitrate addition promoted hydrocarbon degradation and undominated processes; • Pseudomonas can improve oil recovery by producing rhamnolipid; • Roseovarius -MAGs were the novel taxa oxidizing alkane and producing acetate; • Ca. Bacteroidia could potentially degrade hydrocarbons by fumarate addition. Hydrocarbon–degrading consortia (HDC) play an important role in petroleum exploitation. However, the real composition and metabolic mechanism of HDC in the microbial enhanced oil recovery (MEOR) process remain unclear. By combining 13C–DNA stable isotope probing microcosms with metagenomics, some newly reported phyla, including Chloroflexi, Synergistetes, Thermotogae, and Planctomycetes, dominated the HDC in the oil reservoirs. In the field trials, the HDC in the aerobic-facultative-anaerobic stage of oilfields jointly promoted the MEOR process, with monthly oil increments of up to 189 tons. Pseudomonas can improve oil recovery by producing rhamnolipid in the facultative condition. Roseovarius was the novel taxa potentially oxidizing alkane and producing acetate to improve oil porosity and permeability in the aerobic condition. Ca. Bacteroidia were the new members potentially degrading hydrocarbons by fumarate addition in the anaerobic environment. Comprehensive identification of the active HDC in oil reservoirs provides a novel theoretical basis for oilfield regulatory scheme. [ABSTRACT FROM AUTHOR]