Aromatic pollutants rewire soil microbial carbon fixation via chain elongation

Widespread aromatic pollutants such as benzene, toluene, ethylbenzene, and xylene are traditionally considered to drive soil carbon loss through mineralization and ecotoxicity. Contrary to this view, our study reveals that low concentrations of these pollutants stimulate microbial carbon chain elongation-a previously overlooked carbon conversion pathway producing medium-chain fatty acids, thereby reshaping soil carbon dynamics. Using phased amplicon sequencing, metagenomics, and metaproteomics of soil microcosms amended with these compounds, we demonstrate that aromatic pollutants bidirectionally regulate carbon chain elongation at both taxonomic and molecular levels. These pollutants selectively enrich Clostridium sensu stricto 12 and Rummelibacillus while suppressing Acinetobacter, a key elongation taxon in natural soils. Simultaneously, they inhibit Petrimonas, a syntrophic fatty acid degrader, enhancing medium-chain fatty acids accumulation. Carbon chain elongating bacteria cooperate with aromatic degraders, redirecting pollutant-derived carbon towards chain elongation rather than complete mineralization to CO₂. Among them, Bacillus occupies a pivotal niche bridging aromatic degradation and carbon elongation. At the molecular level, aromatic pollutants enhance chain elongation by accelerating substrate uptake and channeling acetyl-CoA into the reverse β-oxidation pathway. Additionally, aromatic pollutants inhibit the fatty acid biosynthesis pathway by upregulating fabR and down-regulating acrR and fadR. They also maintain NADH availability to alleviate Rex-mediated repression of bcd, a critical gene in the β-oxidation pathway. However, high concentrations of aromatic pollutants disrupt metabolic homeostasis and suppress chain elongation activity. Our findings redefine the ecological impact of aromatic hydrocarbon contamination in soil, demonstrating their role in modulating anaerobic carbon fixation and retention within soil microbial communities.