Bacterial benz(a)anthracene catabolic networks in contaminated soils and their modulation by other co-occurring HMW-PAHs

• Published in: Environmental pollution (1987) 2023-07, Vol.328, p.121624-121624, Article 121624
• Main Authors: Jiménez-Volkerink, Sara N., Jordán, Maria, Singleton, David R., Grifoll, Magdalena, Vila, Joaquim
• Format: Article
• Language: English
• Subjects: Benz(a)anthracene; Benz(a)Anthracenes - metabolism; Biodegradation; Biodegradation, Environmental; DNA Stable Isotope Probing; High molecular weight PAHs; Metagenomics; Microbial interactions; Molecular Weight; Polycyclic Aromatic Hydrocarbons - metabolism; Soil; Soil Microbiology; Soil Pollutants - metabolism; Sphingomonadaceae - genetics; Sphingomonadaceae - metabolism
• ISSN: 0269-7491; 1873-6424
• DOI: 10.1016/j.envpol.2023.121624

Polycyclic aromatic hydrocarbons (PAHs) are major environmental pollutants in a number of point source contaminated sites, where they are found embedded in complex mixtures containing different polyaromatic compounds. The application of bioremediation technologies is often constrained by unpredictable end-point concentrations enriched in recalcitrant high molecular weight (HMW)-PAHs. The aim of this study was to elucidate the microbial populations and potential interactions involved in the biodegradation of benz(a)anthracene (BaA) in PAH-contaminated soils. The combination of DNA stable isotope probing (DNA-SIP) and shotgun metagenomics of 13C-labeled DNA identified a member of the recently described genus Immundisolibacter as the key BaA-degrading population. Analysis of the corresponding metagenome assembled genome (MAG) revealed a highly conserved and unique genetic organization in this genus, including novel aromatic ring-hydroxylating dioxygenases (RHD). The influence of other HMW-PAHs on BaA degradation was ascertained in soil microcosms spiked with BaA and fluoranthene (FT), pyrene (PY) or chrysene (CHY) in binary mixtures. The co-occurrence of PAHs resulted in a significant delay in the removal of PAHs that were more resistant to biodegradation, and this delay was associated with relevant microbial interactions. Members of Immundisolibacter, associated with the biodegradation of BaA and CHY, were outcompeted by Sphingobium and Mycobacterium, triggered by the presence of FT and PY, respectively. Our findings highlight that interacting microbial populations modulate the fate of PAHs during the biodegradation of contaminant mixtures in soils. [Display omitted] •DNA-SIP and shotgun metagenomics revealed Immundisolibacter as the main BaA degrader.•Immundisolibacter MAG presented unique genetic organization and atypical RHD.•Biodegradation of target HMW-PAHs was associated with specific key microbial players.•Co-occurrence of HMW-PAHs delayed the removal of the less biodegradable PAHs.•Soil microbial interactive processes modulated the preferential utilization of PAHs.