Multi-Omic Profiling of a Newly Isolated Oxy-PAH Degrading Specialist from PAH-Contaminated Soil Reveals Bacterial Mechanisms to Mitigate the Risk Posed by Polar Transformation Products

Abstract

Polar biotransformation products have been identified as causative agents for the eventual increase in genotoxicity observed after the bioremediation of PAH-contaminated soils. Their further biodegradation has been described under certain biostimulation conditions; however, the underlying microorganisms and mechanisms remain to be elucidated. 9,10-Anthraquinone (ANTQ), a transformation product from anthracene (ANT), is the most commonly detected oxygenated PAH (oxy-PAH) in contaminated soils. Sand-in-liquid microcosms inoculated with creosote-contaminated soil revealed the existence of a specialized ANTQ degrading community, and Sphingobium sp. AntQ-1 was isolated for its ability to grow on this oxy-PAH. Combining the metabolomic, genomic, and transcriptomic analyses of strain AntQ-1, we comprehensively reconstructed the ANTQ biodegradation pathway. Novel mechanisms for polyaromatic compound degradation were revealed, involving the cleavage of the central ring catalyzed by Baeyer–Villiger monooxygenases (BVMO). Abundance of strain AntQ-1 16S rRNA and its BVMO genes in the sand-in-liquid microcosms correlated with maximum ANTQ biodegradation rates, supporting the environmental relevance of this mechanism. Our results demonstrate the existence of highly specialized microbial communities in contaminated soils responsible for processing oxy-PAHs accumulated by primary degraders. Also, they underscore the key role that BVMO may play as a detoxification mechanism to mitigate the risk posed by oxy-PAH formation during bioremediation of PAH-contaminated soils.

Deciphering Microbe-Mediated Dissolved Organic Matter Reactome in Wastewater Treatment Plants Using Directed Paired Mass Distance

“…Those “indirect” links suggest oxygenation, dehydrogenation, hydrogenation, demethylation, and hydration as the potential limiting steps in multiple-step reactions. Oxidases are known to promote ring cleavage of aromatics and are usually found as the first step for lignin and aromatics degradation in environments. , Oxygenation increases the reactivity of DOM and facilitates its utilization by secondary degraders . Besides oxygenation, the rest of the reactions have also been recorded as the major mechanisms related to the degradation of refractory DOM, such as norgestrel and those from landfill leachates .…”

Metagenomic analysis of ready biodegradability tests to ascertain the relationship between microbiota and the biodegradability of test chemicals

“…Therefore, it was revealed that more species of bacteria could be detected as potential degraders of DF by increasing the volume of the test medium. In the case of 2-EA ( 39) such as Terrimonas genus, and Comamonadaceae; Hydrogenophaga previously described, Pseudomonas sp., Gordonialike strain BP9, Mycobacterium gilvum VF1, Nocardioides. [40][41][42][43] Since these substances were considered to have similar metabolic pathways, 39,[44][45][46] it appeared that these bacteria could degrade 2-EA.…”

“…In the case of 2-EA ( 39) such as Terrimonas genus, and Comamonadaceae; Hydrogenophaga previously described, Pseudomonas sp., Gordonialike strain BP9, Mycobacterium gilvum VF1, Nocardioides. [40][41][42][43] Since these substances were considered to have similar metabolic pathways, 39,[44][45][46] it appeared that these bacteria could degrade 2-EA. In addition, in the control tests where 2-EA was not added, the relative abundances of GU454926 and AF358012 were only 1.7 and 1.0%, respectively, and other species were not detected (less than 0.1%), suggesting that these species contributed to the biodegradation of 2-EA and would be potential degraders of 2-EA.…”

Bioremediation of common high-molecular-weight polycyclic aromatic hydrocarbons: a bibliometric analysis based on Web of Science via VOSviewer

“…Oxidized PAHs exhibit potential genotoxicity, causing damage to cells and DNA(Clerge et al, 2023b), and PAH contamination in sh products could potentially pose toxicity to human health through the food chain (de Pinho et al, 2023). In addition, during the bioremediation process, PAHs may generate toxic degradation products(Bonatti et al, 2023;Gou et al, 2023;Jimenez-Volkerink et al, 2023). However, current research is predominantly focused on the evaluation or degradation of LMW-PAHs, such as phenanthrene, anthracene, and naphthalene, with fewer detailed studies on the toxicity and degradation products of HMW-PAHs.…”